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Dieback and decline pathogens of olive trees in South Africa
Abstract
Trunk disease fungal pathogens reduce olive production globally by causing cankers, dieback, and other decline-related symptoms on olive trees. Very few fungi have been reported in association with olive dieback and decline in South Africa. Many of the fungal species reported from symptomatic olive trees in other countries have broad host ranges and are known to occur on other woody host plants in the Western Cape province, the main olive production region of South Africa. This survey investigated the diversity of fungi and symptoms associated with olive dieback and decline in South Africa. Isolations were made from internal wood symptoms of 145 European and 42 wild olive trees sampled in 10 and 9 districts, respectively. A total of 99 taxa were identified among 440 fungal isolates using combinations of morphological and molecular techniques. A new species of Pseudophaeomoniella, P. globosa, had the highest incidence, being recovered from 42.8 % of European and 54.8 % of wild olive samples. This species was recovered from 9 of the 10 districts where European olive trees were sampled and from all districts where wild olive trees were sampled. Members of the Phaeomoniellales (mainly P. globosa) were the most prevalent fungi in five of the seven symptom types considered, the only exceptions being twig dieback, where members of the Botryosphaeriaceae were more common, and soft/white rot where only Basidiomycota were recovered. Several of the species identified are known as pathogens of olives or other woody crops either in South Africa or elsewhere in the world, including species of Neofusicoccum, Phaeoacremonium, and Pleurostoma richardsiae. However, 81 of the 99 taxa identified have not previously been recorded on olive trees and have unknown interactions with this host. These taxa include one new genus and several putative new species, of which four are formally described as Celerioriella umnquma sp. nov., Pseudophaeomoniella globosa sp. nov., Vredendaliella oleae gen. & sp. nov., and Xenocylindrosporium margaritarum sp. nov.
INTRODUCTION
The first record of European olive (Olea europaea subsp. europaea) in South Africa dates back to Jan van Riebeeck in 1661. The first commercial olive farm was established in Paarl in 1925; however, initial expansion of the olive industry only occurred in the 1970s (Costa 1998). Although the olive industry in South Africa is still relatively small, a rapid expansion occurred during the last 11 yr with a 135 % increase in the area planted to the current 3 190 ha. Frantoio is the most frequently planted oil cultivar, accounting for 849 ha of the production area, while Mission is the most frequently planted dual cultivar (oil and table olives; 643 ha of the production area). Due to the recent growth in the olive industry, most of the olive trees in South Africa are relatively young, with 59 % of the trees aged 11–25 yr and only 6 % older than 25 yr. The main olive production region in South Africa is the Western Cape province (92 % of total plantings), where viticulture is the main agricultural enterprise (Viljoen 2020). This region has a Mediterranean climate with warm, dry summers and cool, wet winters. The indigenous wild olive (O. europaea subsp. cuspidata = O. europaea subsp. africana), a close relative of the European olive, commonly occurs in this region, often in close proximity to European olive orchards.
Research on decline diseases of olive trees has previously been dominated by investigations on Verticillium wilt caused by Verticillium dahliae (Jiménez-Díaz et al. 2012), and olive quick decline syndrome caused by the bacterium Xylella fastidiosa (Martelli et al. 2016). The latter pathogen has thus far only been associated with decline of olive trees in Argentina, Brazil, Italy, and the USA (Saponari et al. 2013, Krugner et al. 2014, Haelterman et al. 2015, Coletta-Filho et al. 2016). On the other hand, Verticillium wilt of olive has been reported in various countries in Europe, North Africa, and Central Asia, as well as in the USA (California) and Australia (Jiménez-Díaz et al. 2012). Neither of these olive tree diseases has been reported in South Africa.
In addition to the above-mentioned pathogens, species of Basidiomycota, Botryosphaeriaceae, Cytospora, Diaporthe, Diatrypaceae, Phaeoacremonium, Phaeomoniellales, and some other fungi such as Comoclathris incompta (= Phoma incompta), and Pleurostoma richardsiae, have also been associated with various decline-related symptoms of olive trees in Croatia, Greece, Italy, New Zealand, Spain, and the USA (Rumbos 1988, 1993, Taylor et al. 2001, Carlucci et al. 2008, 2013, 2015, Moral et al. 2010, 2017, Kaliterna et al. 2012, Nigro et al. 2013, Úrbez-Torres et al. 2013, 2020, Lawrence et al. 2018). Úrbez-Torres et al. (2013) identified 18 fungal species in a survey of fungi causing olive twig and branch dieback in California (USA), of which the Botryosphaeriaceae were found to be the most prevalent, followed by species of Diaporthe and the Diatrypaceae. When inoculated onto olive trees, all of these species caused lesions of various sizes, with the largest being produced by Neofusicoccum mediterraneum, followed by Diplodia mutila (Úrbez-Torres et al. 2013). Moral et al. (2010) also found N. mediterraneum to be an aggressive pathogen when inoculated on olive branches. More recent studies have also associated Cytospora oleicola, C. olivarum, C. plurivora, and C. sorbicola with branch cankers and dieback of olive trees in the USA (Lawrence et al. 2018, Úrbez-Torres et al. 2020). In some counties of California, Úrbez-Torres et al. (2020) recovered Cytospora spp. from almost 30 % of twig dieback and canker samples. Pathogenicity trials illustrated the ability of C. oleicola and C. olivarum to cause lesions when inoculated on olive branches (Úrbez-Torres et al. 2020); however, the reported lesion size was considerably smaller than that reported for some species of Botryosphaeriaceae by Úrbez-Torres et al. (2013). In Italy, Pleurostoma richardsiae, Phaeoacremonium spp., and members of the Botryosphaeriaceae have been identified as the most prevalent fungi associated with olive decline (Carlucci et al. 2013, 2015, Nigro et al. 2013). Carlucci et al. (2013) found Pleurostoma richardsiae to be more aggressive than Neofusicoccum parvum and Phaeoacremonium minimum. In a further study identifying Phaeoacremonium species as the most prevalent fungi on olive trees in Italy, Carlucci et al. (2015) found Phaeoacremonium sicilianum, Pc. minimum, and Pc. italicum to be more virulent than Pc. alvesii, Pc. parasiticum, and Pc. scolyti, although all six species caused significant lesions. Species of the Phaeomoniellales were identified from olive trees and reported to be pathogenic to this host in California and Italy (Carlucci et al. 2008, 2013, 2015, Saponari et al. 2013, Úrbez-Torres et al. 2013, Crous et al. 2015). Carlucci et al. (2008, 2013, 2015) initially reported isolates of Pseudophaeomoniella spp. from olive trees in Italy as Lecythophora lignicola (A. Carlucci pers. comm.). The genus Pseudophaeomoniella currently contains two species (P. oleae and P. oleicola) that were recovered from and shown to be pathogenic to olive trees in Italy (Crous et al. 2015). Úrbez-Torres et al. (2013) recovered Phaeomoniella chlamydospora at low incidences from olives in California, and found it to be weakly pathogenic.
Some other fungi have been recorded at lower incidences or only in incidental reports, but have been shown to cause dieback and decline related symptoms on olive trees. These include Diaporthe foeniculina (reported as Phomopsis sp. groups 1 and 2 by Úrbez-Torres et al. 2013 and as Diaporthe sp. by Moral et al. 2017), Diaporthe rudis, Diatrype oregonensis, Diatrype stigma, Eutypa lata, Ilyonectria destructans, Comoclathris incompta (reported as Phoma incompta), and members of the Basidiomycota, such as Fomitiporia mediterranea, Schizophyllum commune, and Trametes versicolor (Rumbos 1988, 1993, Ivic et al. 2010, Carlucci et al. 2013, Úrbez-Torres et al. 2013, Moral et al. 2017).
No formal survey of European olive dieback pathogens in South Africa has been published to date; however, there are some reports of fungi from decline-related symptoms on the closely related wild olive. Crous et al. (2000) lists three basidiomycete species (Ganoderma lucidum, Phellinus linteus = Fomes yucatanensis, and Phellinus robiniae) in association with wood rot, and Hysterographium fraxini var. oleastri in association with dieback of wild olives in South Africa. Furthermore, Adams et al. (2006) reported the Cytospora pruinosa species complex (= Valsa cypri species complex) on dead twigs of the same host in South Africa. In a recent survey of Phaeoacremonium species in South Africa, Spies et al. (2018) reported Phaeoacremonium africanum, Pc. minimum, Pc. parasiticum, and Pc. scolyti on European olives, and Pc. oleae, Pc. prunicola, Pc. scolyti and Pc. spadicum on wild olives. With the exception of Pc. minimum, Pc. parasiticum, and Pc. scolyti, none of the fungi reported in association with olive decline diseases in other countries had been recorded on Olea europaea in South Africa before. Several of these fungi have, however, been associated with cankers, dieback, and other decline related symptoms of grapevines and fruit trees in the Western Cape province of South Africa. These include Diplodia seriata, Neofusicoccum australe, N. luteum, N. parvum, N. vitifusiforme, Diaporthe foeniculina, Eutypa lata, Ilyonectria destructans, Phaeoacremonium alvesii, Pc. rubrigenum, Pc. sicilianum, Phaeomoniella chlamydospora, Pleurostoma richardsiae, and Schizophyllum commune (Crous et al. 2000, Van Niekerk et al. 2004, Damm et al. 2007, 2008a, Cloete et al. 2011, White et al. 2011a, Moyo et al. 2016, 2018a, b). The occurrence of these fungi on such crops, that are often grown in close proximity to European and wild olive trees, suggests that such pathogens could also contribute to olive dieback and decline in South Africa.
Therefore, the aim of this study was to determine the incidence and distribution of fungi associated with dieback and decline diseases of European and wild olive trees in the Western Cape province of South Africa. Furthermore, the association of some of the higher-level taxa with the internal wood symptoms was investigated, and novel taxa within the Phaeomoniellales were described.
MATERIALS AND METHODS
Sampling and collection of fungal isolates
Symptomatic wood samples of 145 European olive trees (Olea europaea subsp. europaea) were collected from 10 districts (defined according to the Wine of Origin scheme, see http://www.sawis.co.za/cert/download/Districts_-_Jan_2014.pdf) in the Western Cape province of South Africa (Appendix 1). Sampled material consisted of cankerous branches or trunks, twigs showing dieback, and old wounds from pruning or other mechanical damage. Samples were collected in larger commercially producing orchards, as well as non-commercial, abandoned or neglected orchards, and trees in domestic gardens. Additional samples with similar symptoms were collected from 42 wild olive trees in nine districts (Appendix 1). Samples were processed as described by Moyo et al. (2016). In short, samples were cut to reveal internal symptoms that were photographed and marked prior to surface sterilisation (30 s in 70 % ethanol, 2 min in 3 % NaOCl, 30 s in 70 % ethanol) and plating of wood pieces from each marked symptom onto potato dextrose agar (PDA, Biolab, South Africa) containing 250 mg/L chloromycetin. Plates were incubated at 24 °C for 4 wk and inspected every 1–3 d. Emerging hyphae of possible fungal pathogens were transferred to fresh PDA plates to obtain pure isolates for identification. Isolates were stored as colonised agar plugs in sterile water at 4 °C and as colonised agar plugs in sterile 10 % glycerol at -84 °C.
Symptoms from which isolations were made, were classified in seven different types in order to investigate if certain fungi were associated with specific symptoms. Samples of European and wild olives were pooled for this aspect of the investigation. The seven symptom types are depicted in Fig. 1 and included twig dieback (n = 126), dark brown to black discolouration (n = 346), light brown to pink discolouration (n = 280), internal black lines (n = 149), the dark brown or black margin between healthy and discoloured tissue (n = 549), streaking (n = 100) and soft or white rot (n = 6). The recovery of isolates of specific fungi from the different symptom types was recorded and expressed as the percentage of symptoms of each type infected by the Basidiomycota, Botryosphaeriaceae, Cytospora, Diaporthe, Diatrypaceae, Phaeoacremonium, Phaeomoniellales, and Pleurostoma, respectively. Fungi not belonging to these genera, families, orders or classes were treated as a single group (‘Other’ fungi), and symptoms from which no fungi were obtained were also recorded.
Identification of isolates
Isolates were classified in morphological groups based on colony morphology and, in some cases, limited microscopic observations. Cultures morphologically identified as Alternaria, Aspergillus, Aureobasidium, Cladosporium, Epicoccum, Fusarium, Penicillium, and Trichoderma, that are generally not considered as dieback and decline pathogens, were discarded. Of the remaining isolates, representatives from all sampling sites and morphological groups were selected for sequencing of the translation elongation factor 1 alpha (TEF1α) region for the Botryosphaeriaceae, beta-tubulin (TUB2) for Phaeoacremonium, and the internal transcribed spacers ITS1 and ITS2 with the enclosed 5.8S ribosomal RNA gene for all remaining isolates (ITS). DNA was extracted using a CTAB-based protocol as described by Damm et al. (2008a). DNA samples were quantified using a NanoDrop ND-1000 spectrophotometer (NanoDrop Technologies, Wilmington, DE, USA), and diluted to a range of 5–15 ng/μL. PCR amplifications were performed in 10 μL reactions (15 μL for TEF1α) containing 1× KAPA Taq Ready Mix (KAPA Biosystems, Cape Town, South Africa), 0.08 μM of each primer (ITS: ITS5 and ITS4 (White et al. 1990); TEF1α: EF1-728F and EF1-986R (Carbone & Kohn 1999); TUB2: T1 (O’Donnell & Cigelnik 1997) and Bt2b (Glass & Donaldson 1995), and 1 μL DNA. Cycling conditions consisted of 5 min at 94 °C, 40 cycles of denaturation at 94 °C for 30 s, annealing for 30 s (ITS: 55 °C; TEF1α: 54.5 °C; TUB2: 58 °C), extension at 72 °C for 30 s, and final extension for 7 min at 72 °C. Successful amplifications were verified by gel electrophoresis and sequenced directly in one direction using the BigDye Terminator v. 3.1 Cycle Sequencing Kit (PE Biosystems, Foster City, CA, USA). The sequencing product was analysed on an ABI PRISM 3130XL DNA sequencer (Perkin-Elmer, Norwalk, CT, USA) at the Central Analytical Facilities of Stellenbosch University. Trimming and editing of sequences were done with Geneious v. 9.1.7 (http://www.geneious.com, Kearse et al. 2012). Preliminary species identities were obtained by BLAST analyses of sequences against the nucleotide database of GenBank for ITS and TEF1α sequences, and against a custom Phaeoacremonium database containing only reference TUB2 sequences from Gramaje et al. (2015), Ariyawansa et al. (2015), Crous et al. (2016), Da Silva et al. (2017) and Spies et al. (2018). BLAST results were further confirmed through alignment of sequences with relevant reference sequences from GenBank using the MAFFT plugin in Geneious (Katoh & Standley 2013) and phylogenetic analyses. The best fit substitution model for each alignment was estimated under the Akaike information criterion using jModeltest 2 (Darriba et al. 2012). Maximum likelihood analyses were performed using PhyML-MPI (Guindon et al. 2010) with support calculated from 100 bootstrap replicates. Phylogenies were viewed in FigTree v. 1.4.2 (http://tree.bio.ed.ac.uk/software/figtree/). For a limited number of isolates, species were identified using species-specific PCR (Diaporthe foeniculina according to Lesuthu et al. 2019 and the new species of Pseudophaeomoniella according to Van Dyk 2020), DNA fingerprinting (Botryosphaeriaceae according to the protocols of Alves et al. 2007), or the morphology was compared to isolates that had been identified using molecular techniques. Representatives of all recovered species were included in phylogenetic analyses to confirm the inferred identities. All phylogenies are available on TreeBASE (study S26669 and S26950).
Phylogenetic analyses of the Phaeomoniellales
A multi-gene phylogeny was generated for isolates in the Phaeomoniellales in an attempt to resolve the taxonomy of species in this order. Double strand consensus sequences of the actin (ACT), beta-tubulin (TUB2) and translation elongation factor 1-alpha (TEF1α) regions, as well as a fragment of the nuclear ribosomal RNA (rRNA) genes including ITS and the D1–D3 regions of the 28S ribosomal RNA gene (LSU), were generated for selected isolates in the Phaeomoniellales. The ACT, TEF1α and TUB2 regions were amplified using the primers ACT-512F and ACT-783R (Carbone & Kohn 1999), EF1-728F and EF1-986R (Carbone & Kohn 1999), and Bt2a and Bt1b (Glass & Donaldson 1995), respectively. Cycling conditions were as described above, but annealing at 52 °C for ACT and TEF1α and 58 °C for TUB2. For some isolates, ACT was amplified using a touch-down protocol with annealing temperatures decreasing from 66–58 °C in decrements of 2 °C every 5 cycles, followed by 20 cycles of annealing at 55 °C. The nuclear ribosomal RNA regions were amplified as a single fragment using the primers ITS5 (White et al. 1990) and LR7 (Vilgalys & Hester 1990) with cycling conditions as described above, but annealing at 50 °C and extending for 1 minute during every cycle. The ITS-LSU fragment was sequenced using the primers ITS3, ITS4, ITS5, LR0R, LR3, LR6 and LR7 (Vilgalys & Hester 1990, White et al. 1990). The ACT, TEF1α, and TUB2 regions were sequenced using primers used for amplification. Sequences were assembled and edited using Geneious v. 9.1.7 (http://www.geneious.com, Kearse et al. 2012). Relevant reference sequences were obtained from GenBank and aligned with de novo generated data as described above (Table 1). The ITS, 28S, ACT, TEF1α and TUB2 regions were aligned separately and concatenated in Geneious v. 9.1.7 (http://www.geneious.com, Kearse et al. 2012). Maximum likelihood and Bayesian analyses of the concatenated and LSU only datasets were conducted in PhyML-MPI (Guindon et al. 2010) and PhyloBayes-MPI v. 1.8 (Lartillot et al. 2013), respectively. The GTR+I+G model was estimated as either the best fit model or one of the top three performing models for the different individual datasets using the Akaike Information Criterion in jModeltest 2 (Darriba et al. 2012). This model was consequently used for maximum likelihood analysis of the concatenated dataset, as well as the LSU dataset (best fit model), with support calculated from 1 000 bootstrap replicates. Bayesian analyses were performed under the CAT-GTR model. For each analysis, two chains were run for 10 000 (concatenated dataset) or 5 000 iterations (LSU dataset) of which the first 1 800 (concatenated dataset) or 800 (LSU dataset) were discarded as burn-in before assessing convergence using the bpcomp and tracecomp commands. The minimum effective sizes after running these commands were larger than 300 and maxdiff values were less than 0.1, indicating sufficient convergence as per the guidelines set out in the PhyloBayes-MPI manual. All phylogenies are available on TreeBASE (studies S26669 and S26950).
Table 1
Species | Strain1 | Country | Host | GenBank accession numbers | ||||
---|---|---|---|---|---|---|---|---|
ITS | 28S | TEF1α | ACT | TUB2 | ||||
Aequabiliella effusa | CBS 120883T = STE-U 6121 | South Africa | Prunus persica | NR_132005 | GQ154618 | MN861676 | n/a2 | KR260451 |
A. palatina | CBS 145018T = JKI-Ap36 | Germany | spore trap attached to grapevine shoot | MH999506 | MH999529 | n/a | n/a | MK070469 |
Celerioriella dura | CBS 120882T = STE-U 6122 | South Africa | Prunus salicina | NR_132004 | GQ154617 | MN861677 | MT787367 | MW017331 |
Ce. petrophiles | CBS 142115T = CPC 29256 | Australia | Petrophile teretifolia | KY173394 | KY173487 | n/a | n/a | n/a |
Ce. prunicola | CBS 120876T = STE-U 6118 | South Africa | Prunus salicina | NR_132003 | GQ154614 | n/a | MT787368 | KR260453 |
Ce. umnquma | STE-U 8442 = CSN801 | South Africa | Olea europaea subsp. cuspidata | MT791052 | MT797851 | MT787395 | MT787370 | n/a |
CBS 146756T = STE-U 7966 = CSN1091 | South Africa | Olea europaea subsp. europaea | MT791051 | MT797850 | MT787394 | MT787369 | n/a | |
Celothelium cinchonarum | F 17105 f | Costa Rica | n/a | n/a | DQ329020 | n/a | n/a | n/a |
Dolabra nepheliae | CBS 123297 | Puerto Rico | Litchi chinensis | GU345749 | GU332515 | n/a | n/a | n/a |
Minutiella pruni-avium | CBS 145513T | Germany | Prunus avium | MN232957 | MN232925 | n/a | n/a | MN232985 |
M. simplex | CBS 145008T = JKI-Jn27 | Germany | spore trap attached to grapevine shoot | MH999508 | MH999531 | n/a | n/a | MK070471 |
M. tardicola | CBS 121757T = STE-U 6123 | South Africa | Prunus armeniaca | GQ154599 | GQ154619 | MN861680 | MT787371 | KR260454 |
Moristroma germanicum | CBS 145012T = JKI-Feb06 | Germany | spore trap attached to grapevine shoot | MH999512 | MH999535 | n/a | n/a | MK070475 |
Mo. japonicum | BN1674T | Japan | Quercus mongolica var. grossoserrata | AY254052 | AY254052 | n/a | n/a | n/a |
Mo. palatinum | CBS 145010T = JKI-Feb17 | Germany | spore trap attached to grapevine shoot | MH999510 | MH999533 | n/a | n/a | MK070473 |
Mo. quercinum | BN1678T | Sweden | Quercus robur | AY254051 | AY254051 | n/a | n/a | n/a |
Neophaeomoniella constricta | CBS 145015T = JKI-Mz35 | Germany | spore trap attached to grapevine shoot | MH999516 | MH999539 | n/a | n/a | MK070479 |
Np. corymbiae | CBS 145092T | Australia | Corymbia citriodora | MK047457 | MK047507 | n/a | n/a | n/a |
Np. eucalypti | CBS 139919T | USA | Eucalyptus globulus | NR_138001 | KR476782 | n/a | n/a | n/a |
Np. eucalyptigena | CBS 145093T | Australia | Eucalyptus pilularis | NR_161148 | MK047508 | MK047569 | n/a | MK047584 |
Np. niveniae | CBS 131316T | South Africa | Nivenia stokoei | JQ044435 | JQ044454 | MN861682 | n/a | n/a |
STE-U 7959 = CSN742 | South Africa | Olea europaea subsp. cuspidata | MT791053 | n/a | MT787396 | n/a | n/a | |
Np. ossiformis | CBS 145013T = JKI-May03 | Germany | spore trap attached to grapevine shoot | MH999514 | MH999537 | n/a | n/a | MK070477 |
Np. zymoides | CBS 114904T = AW304 | Korea | Pinus densiflora | DQ270242 | DQ270253 | n/a | n/a | KR260455 |
CBS 121168 | South Africa | Prunus salicina | GQ154600 | GQ154620 | MN861679 | n/a | MW017332 | |
STE-U 7960 = CSN743 | South Africa | Olea europaea subsp. cuspidata | MT791054 | n/a | MT787397 | n/a | n/a | |
Paraphaeoisaria alabamensis | CBS 110.77A | USA | Cronartium quercuum f. sp. fusiforme | MH861028 | MH872801 | n/a | n/a | n/a |
CBS 110.77BT | USA | Cronartium quercuum f. sp. fusiforme | MH861029 | n/a | n/a | n/a | n/a | |
Paraphaeomoniella capensis | CBS 123535T | South Africa | Encephalartos altensteinii | NR_137711 | FJ372408 | MN861681 | MT787372 | KR260449 |
Phaeomoniella chlamydospora | CBS 229.95T | Italy | Vitis vinifera | NR_155612 | NG_066265 | n/a | n/a | AF253968 |
CBS 117179 | South Africa | Vitis vinifera | KF764544 | n/a | KF764636 | n/a | KF764683 | |
STE-U 7536 | South Africa | Vitis vinifera | MT791061 | MT797852 | MT787398 | MT787373 | n/a | |
‘Phaeomoniella’ pinifoliorum | CBS 114903T | Korea | Pinus densiflora | DQ270240 | MN861685 | MN861678 | n/a | KR260452 |
Pseudophaeomoniella globosa | STE-U 7946 = CSN18 | South Africa | Olea europaea subsp. cuspidata | MT791062 | n/a | MT787403 | MT787378 | MW017333 |
CBS 146758 = STE-U 7947 = CSN41 | South Africa | Olea europaea subsp. cuspidata | MT791066 | n/a | MT787400 | MT787375 | MW017335 | |
STE-U 7950 = CSN183 | South Africa | Olea europaea subsp. cuspidata | MT791055 | n/a | MT787404 | MT787379 | n/a | |
CBS 146755T = STE-U 7951 = CSN185 | South Africa | Olea europaea subsp. europaea | MT791056 | MT797853 | MT787399 | MT787374 | MW017337 | |
STE-U 7952 = CSN186 | South Africa | Olea europaea subsp. europaea | MT791067 | n/a | MT787405 | MT787380 | n/a | |
CBS 146759 = STE-U 7953 = CSN329 | South Africa | Olea europaea subsp. cuspidata | MT791069 | n/a | MT787401 | MT787376 | n/a | |
STE-U 7954 = CSN334 | South Africa | Olea europaea subsp. cuspidata | MT791068 | n/a | MT787406 | MT787381 | n/a | |
STE-U 7955 = CSN349 | South Africa | Olea europaea subsp. europaea | MT791063 | n/a | MT787407 | MT787382 | n/a | |
STE-U 7956 = CSN386 | South Africa | Olea europaea subsp. cuspidata | MT791057 | n/a | MT787408 | MT787383 | n/a | |
STE-U 7957 = CSN435 | South Africa | Olea europaea subsp. europaea | MT791064 | n/a | MT787409 | MT787384 | n/a | |
STE-U 7958 = CSN451 | South Africa | Olea europaea subsp. europaea | MT791058 | n/a | MT787410 | MT787385 | n/a | |
STE-U 7962 = CSN806 | South Africa | Olea europaea subsp. cuspidata | MT791059 | n/a | MT787411 | MT787386 | n/a | |
STE-U 7963 = CSN808 | South Africa | Olea europaea subsp. europaea | MT791070 | n/a | MT787412 | MT787387 | n/a | |
STE-U 7964 = CSN824 | South Africa | Olea europaea subsp. europaea | MT791065 | n/a | MT787413 | MT787388 | n/a | |
STE-U 7965 = CSN960 | South Africa | Olea europaea subsp. europaea | MT791071 | n/a | MT787414 | MT787389 | n/a | |
STE-U 7968 = PMM1192 | South Africa | Olea europaea subsp. europaea | MT791060 | n/a | MT787415 | MT787390 | MW017338 | |
PMM2484 | South Africa | Olea europaea subsp. cuspidata | MT791072 | n/a | MT787402 | MT787377 | n/a | |
P. oleae | CBS 139191T = FV84 | Italy | Olea europaea subsp. europaea | NR_137966 | KP635971 | KP635968 | KP635974 | n/a |
P. oleicola | CBS 139192T = M24 | Italy | Olea europaea subsp. europaea | NR_137965 | KP635970 | KP411802 | KP411805 | n/a |
STE-U 7933 = Ph58 | Italy | Olea europaea subsp. europaea | MW008603 | n/a | MW017340 | MW017339 | MW017336 | |
Rhynchostoma proteae | CBS 112051T | South Africa | Protea laurifolia | NR_132824 | MN861683 | n/a | MT787391 | n/a |
Strelitziana cliviae | CBS 133577T = CPC 19822 | South Africa | Clivia miniata | NR_111823 | NG_042750 | n/a | n/a | n/a |
S. malaysiana | CBS 139902T = CPC 24874 | Malaysia | Acacia mangium | KR476731 | KR476766 | n/a | n/a | n/a |
Vredendaliella oleae | CBS 146757T = STE-U 7969 = PMM1193 | South Africa | Olea europaea subsp. europaea | MT791073 | MT797854 | MT787416 | n/a | MW017334 |
Xenocylindrosporium kirstenboschense | CBS 125545T | South Africa | Encephalartos friderici-guilielmi | NR_132841 | GU229891 | n/a | n/a | n/a |
X. margaritarum | CBS 146848T = STE-U 9059 = CSN1179 | South Africa | Olea europaea subsp. europaea | MT791074 | MT797855 | MT787418 | MT787393 | n/a |
CBS 146849 = STE-U 8437 = CSN1216 | South Africa | Olea europaea subsp. europaea | MT791075 | n/a | MT787417 | n/a | n/a | |
CBS 146850 = STE-U 8440 = CSN1917 | South Africa | Olea europaea subsp. cuspidata | MT791076 | n/a | n/a | MT787392 | n/a | |
X. sp. CFJS-2015c | CSN1180 | South Africa | Olea europaea subsp. europaea | MT791077 | MT797849 | n/a | n/a | n/a |
STE-U 8441 = CSN1184 | South Africa | Olea europaea subsp. europaea | MT791078 | MT797848 | MT787420 | n/a | n/a | |
STE-U 8436 = CSN1203 | South Africa | Olea europaea subsp. europaea | MT791080 | n/a | MT787419 | n/a | n/a | |
X. sp. CFJS-2015e | STE-U 8438 = CSN1222 | South Africa | Olea europaea subsp. europaea | MT791079 | MT797847 | MT787421 | n/a | n/a |
X. sp. CFJS-2015f | STE-U 8435 = CSN1191 | South Africa | Olea europaea subsp. europaea | MT791082 | MT797856 | MT787422 | n/a | n/a |
X. sp. CFJS-2015g | STE-U 8446 = CSN1174 | South Africa | Olea europaea subsp. europaea | MT791081 | MT797846 | n/a | n/a | n/a |
1CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands; CPC: Culture collection of Pedro Crous, housed at CBS; CSN: collection of Chris Spies at ARC-Nietvoorbij, Stellenbosch, South Africa; PMM: collection of Providence Moyo at the University of Stellenbosch, Department of Plant Pathology, Stellenbosch, South Africa; STE-U: fungal collection of the University of Stellenbosch, Department of Plant Pathology; T Ex-type strains.
2Not available.
Morphological characterisation of putative new species in the Phaeomoniellales
Representative isolates of putative new species in the Phaeomoniellales were selected for characterisation of micromorphological structures using a slide culture technique similar to that of Arzanlou et al. (2007). Colonised agar plugs (5–10 × 5–10 mm) were taken from 2-wk-old PDA cultures, placed on autoclaved microscope slides in Petri dishes containing two 90 mm filter paper disks moistened with 1.5 mL sterile deionised water, covered with autoclaved cover slips, and incubated at 25 °C for 10 d. Colonised microscope slides and cover slips were mounted separately in 70 % lactic acid, pressed for several hours to overnight under stacks of heavy books, and sealed with nail polish. Fungal growth on slides was inspected using a Nikon Eclipse Ni light microscope. Isolates were also grown on synthetic nutrient-poor agar (SNA) with autoclaved pine needles (Nirenberg 1976) for the production of conidiomata. Isolates of species that failed to produce conidia under these conditions were also cultured on SNA with autoclaved olive leaves and twigs in an attempt to induce sporulation. Images of vegetative hyphae, conidia, conidiogenous cells, collarettes, and conidiophores were captured at 1 000× and pycnidia at 11.25× magnification using a Nikon DS-Ri2 camera on a Nikon Eclipse Ni light microscope and a Nikon SMZ1500 stereo microscope, respectively. Ten pycnidia and thirty individual structures of each type were viewed and measured using the NIS-Elements Viewer software (Nikon Instruments Inc.).
Colony morphology was evaluated on malt extract agar (MEA, Biolab), oatmeal agar (OA, Biolab) and PDA. Plates of the different media were inoculated with 4 mm diam plugs taken from actively growing PDA cultures and incubated at 25 °C in the dark for 21 d. In some cases, 4 mm diam plugs could not be used due to small colony sizes. For these species 1–2 mm diam colonies were picked from streaked cultures on PDA and transferred to the different media. Colony colours were evaluated using the colour charts of Rayner (1970).
Cardinal temperatures for growth were determined by incubating PDA plates at 25 °C in the dark for 2 d before marking colony margins on the bottom of each plate and incubating them at temperatures ranging from 5–40 °C at intervals of 5 °C in the dark. Each isolate was plated in triplicate for each temperature. Colony margins were marked on the bottom of each plate after 2, 3, and 4 wk. Plates that did not exhibit growth after 4 wk were incubated at 25 °C for an additional 7 d to establish viability of the cultures.
RESULTS
Sampling and collection of fungal isolates
Despite the presence of internal wood discolouration and other symptoms suggesting infection by pathogens in all samples, 43 European olive (30 %) and 12 wild olive (29 %) samples yielded no cultures of the fungi targeted in this survey. Some of these samples yielded putative saprophytes or endophytes that were not recorded; however, more often such samples yielded no fungi. Of the cultures recovered from the remaining samples, 440 representative isolates were identified to species level using sequencing and phylogenetic analyses (389 isolates), sequencing and BLAST (three isolates), DNA fingerprinting (six isolates), species-specific primers (seven isolates) or based on their morphological similarity to other sequenced isolates (25 isolates) (Appendix 2).
The incidence of fungi varied between the different symptom types, with twig dieback showing the highest incidence (63 % infection) while the lowest incidence was recorded for light brown or pink discolouration (21 % infection) (Table 2). All higher-level fungal taxa considered were recovered from all symptom types, except for streaking (no Botryosphaeriaceae, Cytospora, or Diaporthe), twig dieback (no Basidiomycetes, Diatrypaceae, or Pleurostoma) and soft and white rot (only Basidiomycetes recovered). For each symptom type the incidence of symptoms yielding no fungi was higher than the incidence of any of the fungal taxa taken into consideration. The only exception to this was soft and white rot, where only six symptoms were considered of which half yielded no fungi, and the other half yielded Basidiomycota. The Phaeomoniellales had the highest incidence of all higher-level fungal taxa in all symptom types except for soft and white rot, where only Basidiomycota were recovered and twig dieback, where the Botryosphaeriaceae and ‘Other’ fungi had higher incidences (24 % and 27 %, respectively vs 17 % for the Phaeomoniellales). The highest incidence of the Phaeomoniellales was recorded for internal black lines (41 %), followed by streaking (33 %), dark brown or black discolouration (29 %), dark brown or black margins (25 %), twig dieback (17 %), and light brown or pink discolouration (14 %) (Table 2). Twig dieback yielded the highest incidences of Botryosphaeriaceae (23.8 %), Diaporthe (7.1 %), Phaeoacremonium (10.3 %), and ‘Other’ fungi (27.0 %).
Table 2
Fungal group | Streaking (n=100) | Twig dieback (n=126) | Soft/white rot (n=6) | Dark brown or black margin (n=549) | Internal black lines (n=149) | Light brown or pink discolouration (n=280) | Dark brown or black discolouration (n=346) | |||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Basidiomycota | 2 | (2.0 %) | – | 3 | (50.0 %) | 10 | (1.8 %) | 6 | (4.0 %) | 3 | (1.1 %) | 17 | (4.9 %) | |
Botryosphaeriaceae | – | 30 | (23.8 %) | – | 15 | (2.7 %) | 8 | (5.4 %) | 8 | (2.9 %) | 9 | (2.6 %) | ||
Cytospora | – | 1 | (0.8 %) | – | 12 | (2.2 %) | 3 | (2.0 %) | 2 | (0.7 %) | 7 | (2.0 %) | ||
Diaporthe | – | 9 | (7.1 %) | – | 5 | (0.9 %) | 2 | (1.3 %) | 2 | (0.7 %) | 8 | (2.3 %) | ||
Diatrypaceae | 1 | (1.0 %) | – | – | 10 | (1.8 %) | 3 | (2.0 %) | 2 | (0.7 %) | 2 | (0.6 %) | ||
Phaeoacremonium | 2 | (2.0 %) | 13 | (10.3 %) | – | 14 | (2.6 %) | 3 | (2.0 %) | 6 | (2.1 %) | 6 | (1.7 %) | |
Phaeomoniellales | 33 | (33.0 %) | 22 | (17.5 %) | – | 137 | (25.0 %) | 61 | (40.9 %) | 38 | (13.6 %) | 102 | (29.5 %) | |
Pleurostoma | 3 | (3.0 %) | – | – | 10 | (1.8 %) | 6 | (4.0 %) | 2 | (0.7 %) | 9 | (2.6 %) | ||
Other | 4 | (4.0 %) | 34 | (27.0 %) | – | 47 | (8.6 %) | 12 | (8.1 %) | 8 | (2.9 %) | 36 | (10.4 %) | |
No fungi | 60 | (60.0 %) | 47 | (37.3 %) | 3 | (50.0 %) | 341 | (62.1 %) | 73 | (49.0 %) | 220 | (78.6 %) | 190 | (54.9 %) |
Identification of isolates
The list of isolates identified to species level is summarised in Appendix 2 and maximum likelihood phylogenies supporting these identifications are available on TreeBASE (study S26669). A total of 99 different fungal taxa were identified during this study, of which 85 were recovered from European olive trees, 33 from wild olive trees and 23 from both hosts (Table 3, Appendix 2). Forty-two of the recovered species belonged to higher level fungal taxa often associated with trunk disease or dieback of various hosts. These included the class Basidiomycota (six spp.), the families Botryosphaeriaceae (eight spp.) and Diatrypaceae (two spp.), the order Phaeomoniellales (10 spp.), and the genera Biscogniauxia (one sp.), Cytospora (two spp.), Diaporthe (two spp.), Didymosphaeria (two spp.), Geosmithia (one sp.), Phaeoacremonium (seven spp.), and Pleurostoma (one sp.) (Table 3). All species recovered at incidences of more than 5 % were among the classes, orders, families, or genera mentioned above, except for Coniothyrium ferrarisianum (phylogenetically a species of Didymocyrtis, TreeBASE study S26669 tree Tr125042) that was present on 7.6 % (n = 11) of the European olive trees sampled (Table 3). Based on the percentage of infected samples, the most prevalent fungal species infecting both European and wild olives in the Western Cape province of South Africa is a new species of Pseudophaeomoniella (Table 3). This fungus was isolated from 42.8 % (n = 62) and 54.8 % (n = 23) of the European olive and wild olive samples, respectively. Other fungi from these higher-level taxa that occurred in more than 5 % of the European olive samples were Neofusicoccum cryptoaustrale/stellenboschiana (11.7 %), Diaporthe foeniculina (10.3 %), Neofusicoccum australe (9 %), Phaeoacremonium scolyti (7.6 %), Pleurostoma richardsiae (6.9 %), and Eutypa lata (6.2 %) (Table 3). With the exception of Neofusicoccum australe and Coniothyrium ferrarisianum, all these fungi were also recovered from wild olives, although not always at incidences of 5 % or more. In wild olive samples, the most prevalent fungi after the new Pseudophaeomoniella sp. were Phaeoacremonium oleae (19.1 %), Diaporthe foeniculina (9.5 %), Eutypa lata (9.5 %), Biscogniauxia rosacearum (7.1 %), Neophaeomoniella niveniae (7.1 %), and Pleurostoma richardsiae (7.1 %) (Table 3). With the exception of Phaeoacremonium oleae all these fungi were also recovered from European olives, although not necessarily at incidences of 5 % or more. Several other fungi from fungal groups often associated with trunk disease and dieback in various crops were also recovered from either European or wild olives. These included fungi from the Basidiomycota (Fomitiporella viticola, Peniophora lycii, Phlebia acerina, T. versicolor), the Botryosphaeriaceae (Diplodia seriata, N. vitifusiforme, and four undescribed species), Cytospora (C. sp. WVJ-2015a), Diaporthe (D. ambigua), the Diatrypaceae (Cryptovalsa ampelina), Didymosphaeria (Dy. rubi-ulmifolii and Dy. variabile), Phaeoacremonium (Pc. africanum, Pc. minimum, Pc. parasiticum, Pc. prunicola, and Pc. spadicum) and the Phaeomoniellales (Neophaeomoniella zymoides and six undescribed species) (Table 3).
Table 3
Fungal group | Species | Incidence1 | Number of districts2 | ||||
---|---|---|---|---|---|---|---|
European olive (n=145) | Wild olive (n=42) | European olive (n=10) | Wild olive (n=9) | ||||
Basidiomycota | Fomitiporella sp. (Taxon 1) | 6 | (4.1 %) | – | 3 | – | |
Peniophora lycii | 2 | (1.4 %) | – | 1 | – | ||
Phlebia acerina | 1 | (0.7 %) | – | 1 | – | ||
Punctularia atropurpurascens | – | 2 | (4.8 %) | – | 2 | ||
Schizophyllum commune | 4 | (2.8 %) | – | 3 | – | ||
Trametes versicolor | 2 | (1.4 %) | – | 2 | – | ||
Biscogniauxia | Biscogniauxia rosacearum | 2 | (1.4 %) | 3 | (7.1 %) | 1 | 2 |
Botryosphaeriaceae | Diplodia seriata | 3 | (2.1 %) | – | 3 | – | |
Neofusicoccum australe | 13 | (9.0 %) | – | 4 | – | ||
Neofusicoccum cryptoaustrale/stellenboschiana | 17 | (11.7 %) | 1 | (2.4 %) | 3 | 1 | |
Neofusicoccum sp. 4 | 1 | (0.7 %) | – | 1 | – | ||
Neofusicoccum sp. 8 | 2 | (1.4 %) | – | 1 | – | ||
Neofusicoccum sp. PMM-2014a | 1 | (0.7 %) | – | 1 | – | ||
Neofusicoccum sp. WvJ-2015a | 4 | (2.8 %) | 1 | (2.4 %) | 4 | 1 | |
Neofusicoccum vitifusiforme | 1 | (0.7 %) | 1 | (2.4 %) | 1 | 1 | |
Coniothyrium s.lat. | Coniothyrium ferrarisianum 3 | 11 | (7.6 %) | – | 3 | – | |
Cytospora | Cytospora pruinosa | 6 | (4.1 %) | 1 | (2.4 %) | 3 | 1 |
Cytospora sp. WvJ-2015a | 6 | (4.1 %) | – | 3 | – | ||
Diaporthe | Diaporthe ambigua | 1 | (0.7 %) | – | 1 | – | |
Diaporthe foeniculina | 15 | (10.3 %) | 4 | (9.5 %) | 6 | 3 | |
Diatrypaceae | Cryptovalsa ampelina | 1 | (0.7 %) | – | 1 | – | |
Eutypa lata | 9 | (6.2 %) | 4 | (9.5 %) | 4 | 2 | |
Didymosphaeria | Didymosphaeria rubi-ulmifolii | 1 | (0.7 %) | 1 | (2.4 %) | 1 | 1 |
Didymosphaeria variabile | 2 | (1.4 %) | – | 2 | – | ||
Geosmithia | Geosmithia sp. CFJS-2015a | 2 | (1.4 %) | 1 | (2.4 %) | 2 | 1 |
Phaeoacremonium | Phaeoacremonium africanum | 1 | (0.7 %) | – | 1 | – | |
Phaeoacremonium minimum | 1 | (0.7 %) | – | 1 | – | ||
Phaeoacremonium oleae | – | 8 | (19 %) | – | 6 | ||
Phaeoacremonium parasiticum | 3 | (2.1 %) | – | 2 | – | ||
Phaeoacremonium prunicola | – | 1 | (2.4 %) | – | 1 | ||
Phaeoacremonium scolyti | 11 | (7.6 %) | 1 | (2.4 %) | 3 | 1 | |
Phaeoacremonium spadicum | – | 1 | (2.4 %) | – | 1 | ||
Phaeomoniellales | Celerioriella umnquma | 5 | (3.4 %) | 1 | (2.4 %) | 3 | 1 |
Neophaeomoniella niveniae | 1 | (0.7 %) | 3 | (7.1 %) | 1 | 2 | |
Neophaeomoniella zymoides | 2 | (1.4 %) | 1 | (2.4 %) | 2 | 1 | |
Pseudophaeomoniella globosa | 62 | (42.8 %) | 23 | (54.8 %) | 9 | 9 | |
Vredendaliella oleae | 1 | (0.7 %) | – | 1 | – | ||
Xenocylindrosporium margaritarum | 2 | (1.4 %) | 1 | (2.4 %) | 2 | 1 | |
Xenocylindrosporium sp. CFJS-2015c | 3 | (2.1 %) | – | 3 | – | ||
Xenocylindrosporium sp. CFJS-2015e | 1 | (0.7 %) | – | 1 | – | ||
Xenocylindrosporium sp. CFJS-2015f | 1 | (0.7 %) | – | 1 | – | ||
Xenocylindrosporium sp. CFJS-2015g | 1 | (0.7 %) | – | 1 | – | ||
Pleurostoma | Pleurostoma richardsiae | 10 | (6.9 %) | 3 | (7.1 %) | 5 | 3 |
1Incidence values represent numbers of infected trees followed by percentages in parentheses.
2Districts sampled include Calitzdorp, Ceres Plateau, Franschhoek (wild olives only), Lutzville Valley, Paarl, Robertson, Stellenbosch Swartland (European olives only), Tygerberg, Walker Bay (European olives only), Wellington (wild olives only), and Worcester (European olives only). The numbers of samples collected in each district are indicated in Appendix 1.
3Phylogenetically this species groups within the genus Didymocyrtis (see TreeBASE study S26669, tree Tr125042).
Most of the remaining fungal species not belonging to the higher-level taxa mentioned above occurred at incidences lower than 3 %. Exceptions include Mycocalicium victoriae (3.4 % on European olives, not recovered from wild olives) and Teichospora sp. CFJS-2015a (4.8 % on wild olives, not recovered from European olives) (Appendix 2).
Phylogenetic analyses of the Phaeomoniellales
Phylogenetic analyses of the LSU region of the Phaeomoniellales provided good support (≥ 96 % bootstrap support, ≥ 0.97 posterior probability) for most genera included, the only exceptions being Celerioriella that had low support (< 60 % bootstrap support, < 0.6 posterior probability) and Xenocylindrosporium that only had moderate support in the maximum likelihood analysis (71 %), but good support in Bayesian analysis (0.98 posterior probability) (Fig. 2). Strain PMM1193 grouped with Celothelium cinchonarum with strong support in Bayesian analysis (0.99 posterior probability); however, this relationship only had low bootstrap support in maximum likelihood analysis (61 %), and Ct. cinchonarum was positioned on a long branch, indicating considerable phylogenetic distance between PMM1193 and that species (Fig. 2). The concatenated ITS-LSU-ACT-TEF1α-TUB2 phylogeny supported the initial identification of Phaeomoniellales strains collected during this survey based on ITS (TreeBASE study S26669, tree Tr125034). Most strains of the Phaeomoniellales collected in this study and included in the multi-gene phylogeny grouped in six well-supported clades, with four strains occupying unique positions (Fig. 3). Seventeen strains formed a strongly supported clade (98 % bootstrap support, 1.00 posterior probability) that did not include any reference sequences, but was related to Pseudophaeomoniella oleae and Pseudophaeomoniella oleicola. Strains CSN801 and CSN1091 formed a clade with good support (85 % bootstrap support, 0.98 posterior probability) that was related to, but distinct from Celerioriella petrophiles. Strains CSN743 and CSN742, respectively, grouped in clades containing the type strains of Neophaeomoniella zymoides (100 % bootstrap support, 1.00 posterior probability) and Neophaeomoniella niveniae (98 % bootstrap support, 1.00 posterior probability). Nine strains collected in this study formed a diverse clade with weak support (67 % bootstrap support, 0.73 posterior probability) that did not include any reference sequences, but was related to Xenocylindrosporium kirstenboschense. Within this clade, six isolates formed two clades of three isolates each that had complete support (100 % bootstrap support, 1.00 posterior probability). The remaining three isolates in this clade (CSN1174, CSN1191, and CSN1222) occupied unique positions. As with the LSU phylogeny, strain PMM1193 grouped on its own in a position related to, but distinct from, Celothelium cinchonarum.
TAXONOMY
Celerioriella umnquma C.F.J. Spies, van Jaarsveld, L. Mostert & Halleen, sp. nov. — MycoBank MB836257; Fig. 4
Etymology. Referring to the Xhosa word for the host, olive, umnquma.
Typus. South Africa, Western Cape, Somerset-West, necrotic wood of European olive (Olea europaea subsp. europaea), 10 Mar. 2015, C.F.J. Spies (holotype CBS H-24370, culture ex-type CBS 146756 = STE-U 7966 = CSN1091).
Mycelium smooth-walled to verruculose, hyaline, 1–1.5(–2) (av. 2) μm diam. Pycnidia not observed. Conidia on hyphae borne in slimy heads on intercalary adelophialides and on terminal or lateral phialides. Terminal and lateral phialides smooth-walled, hyaline to pale brown, mainly slender elongate ampulliform to navicular, (8–)8.5–17.5(–19.5) × 1.5–2(–2.5) (av. 13.5 × 2) μm. Adelophialides abundant, mainly cylindrical, sometimes conical or cylindrical with an inflated base, 1–8(–9.5) × 1–2(–3.5) (av. 2.5 × 1.5) μm. Collarettes cylindrical, 0.5–1 × 0.5–1(–1.5) (av. 1 × 1) μm (only 23 measured). Conidia smooth-walled, hyaline, subcylindrical to oblong ellipsoidal, ovoid, obovoid, 2.5–4(–4.5) × 1–2 (av. 3.5 × 1.5) μm. Conidiophores branched or unbranched, up to 4 septa, 15.5–37.5 × 2–2.5 (av. 22.5 × 2) μm (only 12 measured).
Culture characteristics — Colonies on PDA spreading, reaching 20, 31 and 42 mm diam in 2, 3 and 4 wk, respectively; surface smooth, flat, with some central folds, without aerial mycelium, with entire edge, after 3 wk pale rosy buff above and in reverse. On MEA flat, surface smooth with central folds, without aerial mycelium, with entire margin, after 3 wk pale rosy vinaceous above, rosy buff in reverse. On OA flat, with felty aerial mycelia, white with pale hazel sections near the centre and margins of the colony.
Notes — Despite the fact that none of the phylogenies presented provides good support for the Celerioriella clade including Ce. umnquma, this species is included in Celerioriella based on morphological similarities to this genus (e.g., the abundance of adelophialides) and differences to the phylogenetically closely related genera Pseudophaeomoniella that develops a yeast-like synasexual morph in culture (Crous et al. 2015) and Dolabra that has long, fusiform conidia (Rossman et al. 2010). Celerioriella umnquma is phylogenetically related to, but distinct from, Ce. petrophiles. Morphologically, these species can be distinguished based on the thinner hyphae of Ce. umnquma and colony pigmentation on PDA and MEA. The pycnidial conidiomata reported for Ce. petrophiles and other Celerioriella spp. have not been observed in Ce. umnquma. A BLAST search of the ITS region of Ce. umnquma against the Nucleotide database of GenBank revealed probable conspecificity (98–99 % similarity over 419 and 454 bases) with two strains of an unidentified ‘Phaeomoniella’ species recovered from olive twigs in Portugal (KT804064 and KU325017; Gomes et al. 2019). In the current investigation this species was recovered from both European and wild olives, but at low incidences (< 4 %).
Pseudophaeomoniella globosa C.F.J. Spies, Carlucci, Moyo, van Jaarsveld, Halleen & L. Mostert, sp. nov. — MycoBank MB836258; Fig. 5
Etymology. Referring to the globose conidiogenous cells observed in pycnidia produced on olive wood.
Typus. South Africa, Western Cape, Robertson, necrotic wood of European olive (Olea europaea subsp. europaea), 2 Nov. 2014, P. Moyo (holotype CBS H-24369, culture ex-type CBS 146755 = STE-U 7951 = CSN185).
Mycelium smooth-walled to finely verruculose, hyaline, (1–)1.5–2.5 (av. 2) μm diam. Yeast-like growth observed occasionally. Conidia forming on hyphal cells and in pycnidia. Pycnidia produced on pine needles on SNA after incubation for 3–4 wk, (66.5–)67.5–149.5(–151) μm diam, dark brown to black, seemingly opening by irregular rupture, exuding clear conidial suspension, wall of 1–4 layers of brown textura angularis; conidiogenous cells mainly ampulliform, sometimes subcylindrical, navicular, globose to sub-globose, lageniform, pyriform, or irregular shaped, 3.5–9(–10) × 2–4.5 (av. 6 × 3) μm; collarettes inconspicuous, short, cylindrical, 0.5–1.5 × 1–1.5 (av. 1 × 1) μm (only five characterised); conidia smooth-walled, hyaline, subcylindrical to oblong ellipsoidal, 2.5–3 × 1–1.5 (av. 3 × 1) μm. Conidia on hyphae borne in slimy heads on intercalary adelophialides and terminal or lateral phialides, or in rows within empty hyphae (endoconidia). Terminal and lateral phialides mainly elongate ampulliform to subcylindrical with tapering apex, occasionally navicular to ovoid, obovoid or with irregular shape, 4–16.5 × (1–)1.5–3 (av. 8.5 × 2) μm. Adelophialides mainly conical, sometimes subcylindrical or elongate ampulliform, 1–3.5(–4) × 1–3 (av. 2 × 2) μm. Phialides and adelophialides often constricted at the collarette. Collarettes cylindrical, 0.5–1.5 × 0.5–2 (av. 1 × 1) μm (only 18 measured). Conidia smooth-walled, hyaline, subcylindrical to oblong ellipsoidal to obovoid, (2–)2.5–3.5(–4) × 1–2 (av. 3 × 1.5) μm. Endoconidia subcylindrical to oblong ellipsoidal, 2–3.5 × 1–1.5 (av. 3 × 1.5) μm. Conidiophores uncommon, branched or unbranched, up to 3 septa, 7.5–21 × 2–2.5 (av. 13.5 × 2.5) μm (only 4 measured).
Culture characteristics — Colonies on PDA spreading, reaching 25, 37 and 47 mm diam in 2, 3 and 4 wk, respectively; surface smooth, flat, without aerial mycelium, with entire edge, after 3 wk pale buff above and buff to pale honey in reverse. On MEA smooth, flat with some folds in the centre, without aerial mycelium, with entire edge, after 3 wk white above, pale buff with pale honey centre in reverse. On OA smooth with woolly aerial mycelium in the centre, with entire edge, after 3 wk white with greenish olivaceous centre.
Additional materials examined. South Africa, Western Cape, Strand, internal wood necrosis of wild olive (Olea europaea subsp. cuspidata), 25 Sept. 2014, P. Moyo, cultures CBS 146758 = STE-U 7947 = CSN41; Western Cape, Stellenbosch, Jonkershoek, internal wood necrosis of wild olive (Olea europaea subsp. cuspidata), 12 Feb. 2015, C.F.J. Spies, cultures CBS 146759 = STE-U 7953 = CSN329.
Notes — Pseudophaeomoniella globosa is widespread and occurs frequently on European and wild olives in the Western Cape province of South Africa. Phylogenetically, this species is very closely related to P. oleae and P. oleicola. This was also confirmed by a BLAST search using the ITS region. Of the four gene regions used here for phylogenetic analyses, TEF1α provides the highest support for the distinction between the species. Morphologically, P. globosa can be distinguished by the production of endoconidia, which has not been reported for the other species of Pseudophaeomoniella. Strains CSN41 and CSN329 produced phialides and adelophialides with more diverse and irregular shapes than the type strain, e.g., some phialides were sub-globose, ovoid or obovoid. This is reflected in the slightly shorter and wider dimensions recorded for these two strains: 3.5–10.5(–11.5) × (1.5–)2–3(–3.5) (av. 6.5 × 2.5) μm and (3–)3.5–9.5(–10.5) × 2–3(–3.5) (av. 6 × 2.5) μm for strains CSN41 and CSN329, respectively. Hyphae of strain CSN329 sometimes had pale to golden brown pigmentation and individual hyphal segments were sometimes inflated and irregular shaped. Pale brown pigmentation of some phialides was also observed in this strain. Three additional strains were included in studies of culture morphology, but not micromorphology. Strain CSN808 on PDA after 3 wk was pale buff with a pale rosy buff centre and pale vinaceous buff to fawn concentric rings. Pale primrose pigmentation was observed on the PDA colony of CSN960. Some strains had radial folds on PDA and/or MEA. CSN824 on MEA after 3 wk with pale olivaceous buff centre. Strain CSN960 on MEA after 3 wk with concentric folds. Central pigmentation on OA varying from none to sulphur yellow, citrine green, grey olivaceous, pale olivaceous grey, or greenish black.
Vredendaliella C.F.J. Spies, Moyo, Halleen & L. Mostert, gen. nov. — MycoBank MB836261
Etymology. In reference to the location where this genus was first recovered.
Type species. Vredendaliella oleae C.F.J. Spies, Moyo, Halleen & L. Mostert.
Mycelium consisting of hyaline to dark brown septate hyphae. Conidia formed on hyphae and in pycnidia. Conidiogenous cells on hyphae mostly reduced to adelophialides. Conidia borne on slimy heads on conidiogenous cells, aseptate, hyaline, smooth-walled, subcylindrical, oblong-ellipsoidal to obovoid. Conidiomata pycnidial, dark brown to black, semi-immersed or superficial, sub-globose or irregularly shaped. Conidiogenous cells brown, smooth-walled, ellipsoidal to broadly ellipsoidal. Conidia smooth-walled, hyaline, subcylindrical to oblong-ellipsoidal to obovoid.
Vredendaliella oleae C.F.J. Spies, Moyo, Halleen & L. Mostert, sp. nov. — MycoBank MB836263; Fig. 6
Etymology. Referring to the host from which this species was recovered.
Mycelium smooth-walled, forming irregularly swollen hyphal cells on PDA, hyaline, sometimes dark brown, 1–2.5 (av. 1.5) μm. Conidia forming on hyphal cells and in pycnidia. Pycnidia forming on pine needles on SNA after 4 wk, globose to irregularly globose (50–)60.5–160.5(–170.5) (av. 106.5) μm. Seemingly opening by irregular rupture to exude clear conidial suspension. Conidiogenous cells in pycnidia usually dark brown, ellipsoidal to broadly ellipsoidal, oval or lens-shaped, sometimes ampulliform, fusiform or cylindrical, often with bib-like collar, (4.5–)5–11(–12.5) × 2–5 (av. 7.5 × 4) μm; collarettes inconspicuous, cylindrical, 0.5–1.5 × 0.5–1.5 (av. 0.5 × 1) μm (only 11 characterised); conidia smooth-walled, hyaline, ellipsoidal to oblong-ellipsoidal or subcylindrical, 2.5–4.5(–5) × 1.5–2 (av. 3 × 1.5) μm. Conidia on hyphae borne in slimy heads on intercalary adelophialides and terminal or lateral phialides. Terminal and lateral phialides mainly subcylindrical to navicular, (4–)6–12(–14) × 1–3(–3.5) (av. 9 × 2) μm (only 29 measured). Adelophialides mainly subcylindrical, sometimes conical, 1–8 × 1–2.5 (av. 3.5 × 1.5) μm. Collarettes cylindrical, 0.5–1.5 × 1–2 (av. 1 × 1.5) μm (only 9 measured). Conidia smooth-walled, hyaline, subcylindrical to oblong-ellipsoidal to obovoid, 2.5–3.5 × 1–2 (av. 3 × 1.5) μm. Conidiophores uncommon, branched or unbranched, usually brown, up to 1 septum, 8–17 × 1–3.5 (av. 15 × 2.5) μm (only 5 measured).
Culture characteristics — Colonies on PDA slow growing, without aerial mycelium, creased, with undulate margin, after 3 wk white, pale buff in reverse. On MEA restricted, without aerial mycelium, creased, with undulate margin, after 3 wk white above, pale buff in reverse. On OA smooth with sparse woolly mycelium in the centre, with entire margin, after 3 wk white.
Specimens examined. South Africa, Western Cape, Vredendal, necrotic wood of European olive (Olea europaea subsp. europaea), 13 Aug. 2013, P. Moyo (holotype CBS H-24371, culture ex-type CBS 146757 = STE-U 7969 = PMM1193).
Notes — Vredendaliella oleae is currently known only from the ex-type strain reported here. An ITS BLAST search on the Nucleotide database of GenBank revealed that the closest match to this species only had 95 % sequence identity over 483 bases (KP992094), suggesting that there are currently no other records of the ITS region of Vredendaliella oleae on GenBank. The closest BLAST match (KP992094) is of an unclassified Eurotiomycetes species from Juniperus deppeana in the USA (Huang et al. 2016). The LSU phylogeny presented here suggests that Vredendaliella is related to Celothelium as represented by Ct. cinchonarum, although bootstrap support for this relationship is not very strong (61 % bootstrap support, 0.99 posterior probability) and long branch lengths suggests considerable evolutionary distance between the two taxa. Unfortunately, the only sequenced Celothelium species (Ct. aciculiferum and Ct. cinchonarum) are only known from their ascomata (no data are available on conidiomata) and Vredendaliella oleae is currently only known from its conidiomata, since no ascomata were observed in this study. This complicates morphological comparisons between these species. Conidiomata in other Celothelium species are described as pycnidial or stromatic with thin-walled, lageniform conidiogenous cells, and multi-septate, filiform macroconidia, but no microconidia (Aguirre-Hudson 1991). Vredendaliella oleae differs from them in the shape of the conidiogenous cells, absence of macroconidia and presence of microconidia.
Xenocylindrosporium margaritarum C.F.J. Spies, van Jaarsveld, Halleen & L. Mostert, sp. nov. — MycoBank MB836260; Fig. 7
Etymology. Latin, meaning ‘of pearls’, a dual reference to the chains of globose vegetative hyphal cells that resemble strings of pearls, and the location from which the type strain was recovered (Paarl, meaning ‘pearl’).
Typus. South Africa, Western Cape, Paarl, necrotic wood of European olive (Olea europaea subsp. europaea), 4 Feb. 2015, C.F.J. Spies (holotype CBS H-24372, culture ex-type CBS 146848 = STE-U 9059 = CSN1179).
Mycelium on PDA after 4 wk consisting mainly of branched chains of hyaline, smooth-walled, globose to irregular cylindrical hyphal cells, individual hyphal cells sometimes include inflated and non-inflated sections (4.5–)5.5–15.5(–18.5) × (2.5–)3–10(–11) (av. 10 × 5) μm. Hyaline to dark green hyphae consisting of smooth-walled to verruculose cylindrical cells were occasionally observed. Conidia produced on vegetative hyphae. Conidiogenous cells monophialidic, smooth-walled, hyaline, similar in shape and size to vegetative hyphal cells, globose, ampulliform to cylindrical, sometimes with a narrow elongated cylindrical neck, (6–)6.5–14.5(–16.5) × 3–8.5 (av. 10 × 5) μm. Collarettes rarely observed, cylindrical, 0.5–1 × 1–2 (av. 1 ×1.5) μm (only 7 characterised). Conidia solitary, smooth-walled, hyaline, single-celled, curved, tapering to rounded apex and truncate base, (10.5–)12–20(–20.5) × 2–3(–3.5) (av. 16 × 2.5) μm. Swollen conidia becoming septate and differentiating to become vegetative hyphal or conidiogenous cells.
Culture characteristics — Colonies on PDA very slow growing. On MEA without prominent aerial mycelium, irregularly raised, with undulate margin, after 3 wk white and leaden grey above, white and olivaceous grey in reverse. On PDA uneven, irregularly raised, smooth surface, with some felty aerial mycelium, with undulate margin, after 3 wk white and grey olivaceous to iron grey above, white in reverse. On OA raised, felty to woolly aerial mycelium, with entire edge, after 3 wk buff, a clear exudate is produced around the colony.
Notes — This species was recovered from both European and wild olives in this study, but at low incidences (< 3 %). An ITS BLAST on the Nucleotide database of GenBank suggests that there are no other ITS representatives of X. margaritarum on GenBank (closest match < 91.5 % sequence identity over ~ 600 bases). Although generic concepts within the Phaeomoniellales have not been resolved, phylogenetic analyses of the LSU gene region groups X. margaritarum with X. kirstenboschense (type species of Xenocylindrosporium; 71 % bootstrap support, 0.98 posterior probability). Conidiogenous cells and conidia of X. margaritarum also conform to the generic description provided by Crous et al. (2009). Unfortunately, the ex-type strain of X. margaritarum did not produce acervuloid conidiomata typical of the genus when cultured on MEA, PDA, SNA with autoclaved pine needles, SNA with autoclaved olive twigs and leaves, or OA. Alternative culturing methods might be required to induce these structures. Sporulation of the ex-type strain was only observed on PDA after 4 wk. Two additional strains of X. margaritarum (CSN1216 and CSN1917) produced pale buff to pale rosy buff colonies on OA, but exhibited colony morphologies similar to that of the type strain on MEA and PDA. These strains did not sporulate on MEA, PDA, or OA and were not characterised with regards to other micromorphological characteristics.
DISCUSSION
This survey has revealed a unique community of fungi associated with dieback and decline related symptoms on European and wild olive trees in South Africa. On European olive trees, species of the Phaeomoniellales were the most prevalent, being isolated from 48 % of the samples, followed by species of Botryosphaeriaceae (19 %), while all other higher-level fungal taxa including Phaeoacremonium and the Diatrypaceae occurred at incidences of 11 % or less. Similar surveys of fungi associated with wilt, dieback and cankers on European olive trees in Europe and the USA found the dominant fungi to be the Botryosphaeriaceae in Spain and the USA (Úrbez-Torres et al. 2013, Moral et al. 2017) and Phaeoacremonium or the Botryosphaeriaceae in Italy (Carlucci et al. 2013, 2015). Recently published data further suggest that species of Cytospora are also important contributors to cankers and dieback of olive trees in the USA (Úrbez-Torres et al. 2020). There are several possible reasons why the fungi associated with olive dieback and decline in South Africa are so different to those reported in the countries mentioned above. The age of the olive industry and the olive trees planted is likely to be an important contributing factor, since Carlucci et al. (2013, 2015) found higher incidences of some pathogens such as the Botryosphaeriaceae and Phaeoacremonium in older trees (25–35 yr in Carlucci et al. (2013) and > 50 yr in Carlucci et al. (2015)), whereas most South African olive trees are younger than 25 yr. Úrbez-Torres et al. (2020) suggested that climatological conditions and the availability of susceptible hosts may have influenced the distribution of Cytospora species across olive producing counties in California. Similarly, environmental differences between South Africa, the USA and Europe may have contributed to differences in the profiles of fungal species associated with olive decline and dieback. The fact that P. globosa was recovered frequently from both European and indigenous wild olive trees in South Africa, has a wide distribution within the Western Cape province, and has not been reported from any other host or country, suggests that this species might be indigenous to South Africa, with the native wild olive trees as its primary host. However, it is also possible that this species was introduced from abroad along with the European olive host, and has since adopted the indigenous wild olive as a new host. Further studies are required to confirm this.
A surprisingly high number of novel taxa in the Phaeomoniellales were discovered during the current survey. The order Phaeomoniellales was recently introduced by Chen et al. (2015) to accommodate the genera Celothelium, Dolabra, Moristroma, Phaeomoniella, and Xenocylindrosporium. Crous et al. (2015) further split the genus Phaeomoniella into six different genera (Aequabiliella, Celerioriella, Minutiella, Neophaeomoniella, Paraphaeomoniella, and Phaeomoniella), and also introduced Pseudophaeomoniella as a new genus. Phylogenetic relationships among the genera within the Phaeomoniellales have not been resolved (Chen et al. 2015), which complicates the generic classification within this order. None of the gene regions used in our analyses resolved all genus-level relationships with good support. However, phylogenetic analyses of the D1–D3 regions of the LSU region provided moderate to good support for almost all genera in the Phaeomoniellales for which data were included from more than one species, i.e., Moristroma, Neophaeomoniella, Pseudophaeomoniella, and Xenocylindrosporium. The only exception was Celerioriella (Ce. dura, Ce. petrophiles, Ce. prunicola, and Ce. umnquma) that had low support in maximum likelihood and Bayesian analyses. The fact that most genera with more than one species in the Phaeomoniellales were well-supported in phylogenetic analyses of the LSU region suggests that this region is currently adequate for the delineation of genera in the Phaeomoniellales. Kraus et al. (2020) recently described six new species of known genera in the Phaeomoniellales collected in German vineyards. Such collections and descriptions broaden the available knowledge on genera in the Phaeomoniellales and help to consolidate generic concepts within this order. The future discovery and description of taxa in the Phaeomoniellales will no doubt further improve the resolution of evolutionary relationships and generic boundaries among taxa within this order.
Members of the Phaeomoniellales are generally associated with plants as endophytes, saprophytes or plant pathogens (Chen et al. 2015). Species that have been associated with vascular discolouration and other trunk disease or decline symptoms in various hosts include Phaeomoniella chlamydospora (one of the causal agents of Petri disease and esca in grapevines), Aequabiliella effusa, Celerioriella dura, Celerioriella prunicola, Minutiella tardicola, Neophaeomoniella zymoides, Pseudophaeomoniella oleae, and Pseudophaeomoniella oleicola (Larignon & Dubos 1997, Damm et al. 2010, Úrbez-Torres et al. 2013, Crous et al. 2015). Symptom associations in the current survey indicated a high incidence of Phaeomoniellales (mainly Pseudophaeomoniella globosa) in streaking symptoms of European and wild olives (33 % incidence) while all other fungi occurred at low incidences (≤ 4 %) in this symptom type. Similarly, vascular streaking of grapevines and olives have been associated with infections by Phaeomoniella chlamydospora (Mugnai et al. 1999, White et al. 2011b, Úrbez-Torres et al. 2013). The Phaeomoniellales also had high incidences in other symptoms of branches and trunks of European and wild olives where black or dark brown discolouration of the wood was observed (25–41 %). The recently described Pseudophaeomoniella oleae and Pseudophaeomoniella oleicola were both recovered from European olive trees in Italy and reported to cause extensive wood discolouration (Crous et al. 2015). Carlucci et al. (2008) reported the development of brown streaking, chlorosis, loss of leaves and shoot dieback in European olive trees six years after inoculation with a species of Pseudophaeomoniella that had incorrectly been identified as Lecythophora lignicola at the time (Carlucci pers. comm.). Pseudophaeomoniella globosa, the dominant species recovered in the current survey, is closely related to the other two species in this genus. This close evolutionary relationship, together with the wide distribution, high incidence and strong association of P. globosa with internal wood symptoms of olives as observed in the current survey, implicates this species as an important role player in olive dieback and decline in South Africa. Other members of the Phaeomoniellales were recovered at much lower incidences, and only two of the eight species are known (Neophaeomoniella niveniae and Np. zymoides). The only previous record of Np. niveniae is that of the type, which was collected from leaves of Nivenia stokoei, also in the Western Cape Province of South Africa (Crous et al. 2011). The pathogenic ability of this species is unknown. Neophaeomoniella zymoides, although initially reported as an endophyte of pine needles in Korea (Lee et al. 2006), was later associated with necrotic wood of plum trees in South Africa (Limpopo Province), and shown to cause significant lesions when inoculated on peach shoots, but not on plum (Damm et al. 2010). More recently this species was also recovered from spore traps in German vineyards, but found to be non-pathogenic to grapevine (Kraus et al. 2020). Of the remaining Phaeomoniellales species collected from olive trees in this study, one is a new genus here described as Vredendaliella, and five are previously undescribed species of Xenocylindrosporium. Formal descriptions of four of the undescribed species of Xenocylindrosporium were not possible in this study due to a failure of isolates to sporulate on a variety of media. Prior to this study, Xenocylindrosporium was only known from the collection and description of the type species, X. kirstenboschense, from leaf spots of Encephalartos friderici-guilielmi (Crous et al. 2009). Although the culturing techniques and media are not clearly outlined in that study, the production of acervuloid conidiomata was reported on the host material and on MEA. In the current investigation, sporulation of Xenocylindrosporium was successfully induced only on PDA and only in one strain of X. margaritarum. Furthermore, all Xenocylindrosporium isolates exhibited slow to very slow growth on agar media. This suggests alternative culturing techniques or media would probably more ideal for investigating these fungi.
Species of the Botryosphaeriaceae were reported as the most common pathogens associated with olive dieback in the USA (Úrbez-Torres et al. 2013) and Spain (Moral et al. 2017). Species that have been reported from dieback and decline symptoms of European olives in these countries, Croatia, Italy, and New Zealand include Botryosphaeria dothidea, Diplodia mutila, Di. seriata, Dothiorella iberica, Lasiodiplodia theobromae, Neofusicoccum luteum, N. mediterraneum, N. parvum, N. ribis, and N. vitifusiforme (Taylor et al. 2001, Romero et al. 2005, Lazzizera et al. 2008, Moral et al. 2010, 2017, Kaliterna et al. 2012, Carlucci et al. 2013, 2015, Úrbez-Torres et al. 2013). Of these species only Di. seriata and N. vitifusiforme were recovered from olive trees in the current survey, and at very low incidences (1–2 %). Nevertheless, the pathogenicity of both these species to olive trees has been shown (Carlucci et al. 2013, Úrbez-Torres et al. 2013). Neofusicoccum cryptoaustrale/stellenboschiana and N. australe were the most common species of the Botryosphaeriaceae on European olives in this survey. Neofusicoccum australe has been associated with trunk diseases of grapevines, Japanese persimmons and stone fruit in South Africa (Van Niekerk et al. 2004, Damm et al. 2007, Moyo et al. 2016). This species was also reported as one of the causal agents of drupe rot of olives in Italy by Lazzizera et al. (2008). However, a re-examination of some of the isolates revealed them to be N. cryptoaustrale and N. stellenboschiana (Yang et al. 2017). In the current investigation, these two species could not be distinguished using ITS, TEF1α, and TUB2 sequence data alone or in combination. Neofusicoccum cryptoaustrale was originally isolated from Eucalyptus leaves (Crous et al. 2013) and shown to be pathogenic to this host by Pavlic-Zupanc et al. (2017). Neofusicoccum stellenboschiana was described by Yang et al. (2017) using a strain originally isolated from, and shown to be pathogenic to grapevines in South Africa by Van Niekerk et al. (2004). Four undescribed Neofusicoccum species were also recovered during the current survey, but at low incidences. Two of these, Neofusicoccum sp. 4 and Neofusicoccum sp. 8 have, respectively, previously been reported from grapevines and Proteaceae in South Africa (Van Niekerk et al. 2004, Marincowitz et al. 2008, Yang et al. 2017). The Botryosphaeriaceae were the most common fungi isolated from twig dieback symptoms in this survey. This is also in agreement with the results of Úrbez-Torres et al. (2013) who found a considerably higher incidence of Botryosphaeriaceae compared to other fungi in olive twig dieback samples in the USA. However, these authors also found a higher incidence of Botryosphaeriaceae in perennial cankers than in twig dieback samples. In our survey perennial cankers were not assessed as a single symptom type, but isolates of the Botryosphaeriaceae were also recovered from various internal wood symptoms that could have been associated with perennial cankers, although at very low incidences (≤ 5 %).
Diaporthe species have been associated with dieback and decline symptoms of European olives in Italy, Spain, and the USA (Carlucci et al. 2013, Úrbez-Torres et al. 2013, Moral et al. 2017). Aside from D. rudis (reported as D. viticola by Úrbez-Torres et al. 2013), isolates of Diaporthe reported in those surveys were not conclusively identified to the species-level. Both Moral et al. (2017) and Úrbez-Torres et al. (2013) identified some isolates as Diaporthe sp. or Phomopsis sp. groups 1 and 2. However, inclusion of the ITS sequences of those isolates in our Diaporthe phylogeny suggests that these are in fact D. foeniculina. In the current survey, this species was the most prevalent Diaporthe species and the third most prevalent fungus overall on European olives. It was also recovered from three wild olive trees. Úrbez-Torres et al. (2013) found that both D. foeniculina (reported as Phomopsis sp. groups 1 and 2) and D. rudis caused significant lesions on olive branches, but these were considerably smaller than those caused by N. mediterraneum and D. mutila. Moral et al. (2017) on the other hand, reported asymptomatic infections by inoculated D. foeniculina isolates. Diaporthe ambigua has not been reported on olives globally, but has been associated with trunk disease and decline-related symptoms in apple, Japanese persimmon, grapevine, pear and plum trees and grapevines in South Africa (Smit et al. 1996, Van Niekerk et al. 2005, White et al. 2011a, Moyo et al. 2016). This species was only recovered from a single European olive tree during the current survey and its pathogenicity to this host is currently unknown.
All Phaeoacremonium species recorded on European and wild olive trees during this survey were previously reported on these hosts by Spies et al. (2018). Elsewhere in the world, Phaeoacremonium species have been implicated in olive dieback and decline in Italy and the USA (Carlucci et al. 2008, 2013, 2015, Nigro et al. 2013, Úrbez-Torres et al. 2013). Species reported from these countries include Pc. alvesii, Pc. italicum, Pc. minimum, Pc. parasiticum, Pc. rubrigenum, Pc. scolyti, and Pc. sicilianum. In South Africa, Pc. minimum, Pc. parasiticum and Pc. scolyti have also been recovered from European olives (Spies et al. 2018; this study). With the exception of Pc. rubrigenum, all Phaeoacremonium species reported on European olives globally also occur on various woody hosts in South Africa (Mostert et al. 2006, Damm et al. 2008a, Cloete et al. 2011, White et al. 2011a, Moyo et al. 2016, Spies et al. 2018) and the aggressiveness of all species except Pc. rubrigenum has been confirmed on European olive trees (Carlucci et al. 2013, 2015, Úrbez-Torres et al. 2013). The only additional species on European olive in South Africa that have not been reported elsewhere in the world is Pc. africanum (Spies et al. 2018). Prior to that study, Pc. africanum had only been reported from apricot and was shown to be pathogenic to this host as well as to plum (Damm et al. 2008a). In Italy, Carlucci et al. (2013) reported the recovery of Phaeoacremonium (only Pc. minimum) mainly from olive trees older than 25 yr during a survey that included trees aged 18–35 yr. The incidence was not reported as the number of infected trees, but the overall percentage of tissue segments infected by Pc. minimum was low (2.1 %). Two years later, Carlucci et al. (2015) reported high incidences of Phaeoacremonium spp. in olive trees both younger and older than 50 yr (respectively 73 % and 100 % of plants infected) in Italy. Compared to the latter study, the incidences of Phaeoacremonium in European olive trees in South Africa and the USA are quite low (11 % and < 1.8 %, respectively; this study, Úrbez-Torres et al. 2013). One possible explanation for this difference could be the age of the trees, since the majority of European olive trees sampled in the current survey were younger than 25 yr. This could also be a contributing factor to the higher incidence of Phaeoacremonium observed in the wild olive trees during this study, since, although the exact ages are not known, many of these trees appeared to be very old. However, the species of Phaeoacremonium most frequently recovered from wild olives was P. oleae, a species that is not known to occur on European olives, even though these two hosts are often found in close proximity in South Africa.
A wide range of additional fungi were recovered at lower incidences from European and wild olives during the current survey. These include some species reported as olive trunk pathogens elsewhere in the world, such as Cytospora pruinosa complex, Eutypa lata, Pleurostoma richardsiae, Schizophyllum commune, and Trametes versicolor (Rumbos 1993, Carlucci et al. 2008, 2013, 2015, Moral et al. 2010, 2017, Kaliterna et al. 2012, Úrbez-Torres et al. 2013). Several of the remaining fungi, however, have not previously been reported in association with dieback or decline of European olive trees, but are known as dieback or canker pathogens of other woody hosts. Examples of these include Biscogniauxia rosacearum (Raimondo et al. 2016), Cryptovalsa ampelina (Moyo et al. 2018a, b), Didymosphaeria rubi-ulmifolii and Didymosphaeria variabile (Damm et al. 2008b, Cloete et al. 2011). The pathogenicity of these and other fungi recovered in the current survey need to be confirmed on European olive trees in a South African context.
A total of 81 of the 99 fungal taxa identified during this survey had not previously been isolated from olive or wild olive trees globally (Yang et al. 2017, Farr & Rossman continuously updated). Some of these species are known or suspected trunk disease, dieback or decline pathogens of other crops; however, their pathogenicity to olive trees need to be established in order to determine the potential threat these species pose to the olive industry in South Africa. Based on the incidence and distribution of fungi recorded in this survey, P. globosa is likely to be of major concern, if it is shown to be pathogenic.
Acknowledgements
The authors would like to express their gratitude to Palesa Lebenya, Danie Marais, Julia Marais, Bongiwe Sokwaliwa, and Carine Vermeulen for assistance with sampling and isolations. We are also extremely grateful to Maria Luisa Raimondo (University of Foggia, Italy) for providing reference material and sequence data of Pseudophaeomoniella oleicola Ph58. CFJS was supported financially by the Department of Science and Technology (DST) and National Research Foundation (NRF).
Appendix 1 Numbers of European and wild olive samples collected from different districts in the Western Cape Province of South Africa. Districts are defined according to the Wine of Origin scheme, see http://www.sawis.co.za/cert/download/Districts_-_Jan_2014.pdf.
European olive | Wild olive | |
---|---|---|
Calitzdorp | 2 | 2 |
Ceres Plateau | 3 | 4 |
Franschhoek | 0 | 2 |
Lutzville Valley | 24 | 10 |
Paarl | 21 | 1 |
Robertson | 2 | 1 |
Stellenbosch | 27 | 16 |
Swartland | 12 | 0 |
Tygerberg | 14 | 4 |
Walker Bay | 39 | 0 |
Wellington | 0 | 2 |
Worcester | 1 | 0 |
TOTAL | 145 | 42 |
Appendix 2 Species identities, host and location information for 440 fungal strains identified during this survey.
Species | Strain1 | Location | Host | GenBank | Basis for identification2 |
---|---|---|---|---|---|
Anteaglonium sp. CFJS-2015a | CSN641 | Stellenbosch | European olive | MT813895 | TreeBASE S26669, tree Tr125025 |
CSN649 | Stellenbosch | European olive | MT813897 | TreeBASE S26669, tree Tr125025 | |
Anteaglonium sp. CFJS-2015b | CSN642 | Stellenbosch | European olive | MT813896 | TreeBASE S26669, tree Tr125025 |
Biscogniauxia rosacearum | CSN1052 | Stellenbosch | European olive | MT813910 | TreeBASE S26669, tree Tr125028 |
CSN1054 | Wellington | Wild olive | MT813911 | TreeBASE S26669, tree Tr125028 | |
CSN1055 | Wellington | Wild olive | MT813912 | TreeBASE S26669, tree Tr125028 | |
CSN1056 | Stellenbosch | Wild olive | MT813913 | TreeBASE S26669, tree Tr125028 | |
PMM2071 | Stellenbosch | European olive | MT813997 | TreeBASE S26669, tree Tr125028 | |
Calosphaeria africana | CSN33 | Robertson | European olive | MT813858 | TreeBASE S26669, tree Tr125029 |
Capronia sp. CFJS-2015b | CSN1167 | Paarl | European olive | MT813953 | TreeBASE S26669, tree Tr125030 |
CSN1168 | Paarl | European olive | MT813954 | TreeBASE S26669, tree Tr125030 | |
CSN1171 | Stellenbosch | European olive | Not available | Morphological similarity to CSN1172 | |
CSN1172 | Stellenbosch | European olive | MT814032 | TreeBASE S26669, tree Tr125030 | |
Celerioriella umnquma | CSN801 | Durbanville | Wild olive | See Table 1 | Fig. 3 |
CSN1091 | Somerset West | European olive | See Table 1 | Fig. 3 | |
CSN1092 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN1901 | Piketberg | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN1918 | Vredendal | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN1922 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
Clonostachys byssicola | CSN1133 | Durbanville | Wild olive | MT813941 | TreeBASE S26669, tree Tr125032 |
Colletotrichum acutatum | CSN1066 | Durbanville | European olive | MT813920 | TreeBASE S26669, tree Tr125033 |
Coniochaeta decumbens | CSN654 | Durbanville | Wild olive | MT813899 | TreeBASE S26669, tree Tr125035 |
Coniochaeta mutabilis | PMM2016 | Paarl | European olive | MT813987 | TreeBASE S26669, tree Tr125035 |
Coniochaeta velutina | PMM2036 | Stellenbosch | European olive | MT813993 | TreeBASE S26669, tree Tr125035 |
Coniothyrium ferrarisianum | CSN587 | Paarl | European olive | MT813876 | TreeBASE S26669, tree Tr125042 |
CSN588 | Paarl | European olive | MT813877 | TreeBASE S26669, tree Tr125042 | |
CSN590 | Paarl | European olive | MT813878 | TreeBASE S26669, tree Tr125042 | |
CSN632 | Stellenbosch | European olive | MT813893 | TreeBASE S26669, tree Tr125042 | |
CSN1063 | Somerset West | European olive | MT813917 | TreeBASE S26669, tree Tr125042 | |
CSN1064 | Somerset West | European olive | MT813918 | TreeBASE S26669, tree Tr125042 | |
CSN1067 | Somerset West | European olive | MT813921 | TreeBASE S26669, tree Tr125042 | |
CSN1069 | Somerset West | European olive | MT813922 | TreeBASE S26669, tree Tr125042 | |
CSN1070 | Somerset West | European olive | MT813923 | TreeBASE S26669, tree Tr125042 | |
CSN1071 | Durbanville | European olive | MT813924 | TreeBASE S26669, tree Tr125042 | |
CSN1072 | Somerset West | European olive | MT813925 | TreeBASE S26669, tree Tr125042 | |
CSN1073 | Somerset West | European olive | MT813926 | TreeBASE S26669, tree Tr125042 | |
PMM2039 | Stellenbosch | European olive | MT813995 | TreeBASE S26669, tree Tr125042 | |
Cosmospora sp. CFJS-2015a | CSN1162 | Stellenbosch | Wild olive | MT813948 | TreeBASE S26669, tree Tr125036 |
Cryptovalsa ampelina | CSN1924 | Vredendal | European olive | MT813973 | TreeBASE S26669, tree Tr125046 |
Cytospora pruinosa complex | CSN577 | Stellenbosch | European olive | MT813875 | TreeBASE S26669, tree Tr125037 |
CSN623 | Riebeek-Kasteel | European olive | MT814030 | TreeBASE S26669, tree Tr125037 | |
ID0203 | Ceres | Wild olive | MT813983 | TreeBASE S26669, tree Tr125037 | |
PMM2025 | Stellenbosch | European olive | MT814036 | TreeBASE S26669, tree Tr125037 | |
PMM2026 | Stellenbosch | European olive | MT813988 | TreeBASE S26669, tree Tr125037 | |
PMM2029 | Paarl | European olive | MT813989 | TreeBASE S26669, tree Tr125037 | |
PMM2030 | Paarl | European olive | MT813990 | TreeBASE S26669, tree Tr125037 | |
PMM2033 | Stellenbosch | European olive | MT813992 | TreeBASE S26669, tree Tr125037 | |
PMM2077 | Stellenbosch | European olive | MT813999 | TreeBASE S26669, tree Tr125037 | |
Cytospora sp. WvJ-2015a | CSN619 | Stellenbosch | European olive | MT814028 | TreeBASE S26669, tree Tr125037 |
CSN620 | Stellenbosch | European olive | MT813885 | TreeBASE S26669, tree Tr125037 | |
CSN621 | Durbanville | European olive | MT814029 | TreeBASE S26669, tree Tr125037 | |
CSN622 | Stellenbosch | European olive | MT813886 | TreeBASE S26669, tree Tr125037 | |
CSN625 | Stellenbosch | European olive | MT813887 | TreeBASE S26669, tree Tr125037 | |
CSN627 | Stellenbosch | European olive | MT813889 | TreeBASE S26669, tree Tr125037 | |
CSN1153 | Hermanus | European olive | MT813944 | TreeBASE S26669, tree Tr125037 | |
Diaporthe ambigua | PMM2078 | Stellenbosch | European olive | MT814000 | TreeBASE S26669, tree Tr125044 |
Diaporthe foeniculina | CSN223 | Calitzdorp | European olive | MT814020 | TreeBASE S26669, tree Tr125044 |
CSN224 | Franschhoek | Wild olive | MT814021 | TreeBASE S26669, tree Tr125044 | |
CSN225 | Franschhoek | Wild olive | MT814022 | TreeBASE S26669, tree Tr125044 | |
CSN296 | Durbanville | European olive | MT813863 | TreeBASE S26669, tree Tr125044 | |
CSN297 | Durbanville | European olive | MT813864 | TreeBASE S26669, tree Tr125044 | |
CSN301 | Durbanville | European olive | MT814023 | TreeBASE S26669, tree Tr125044 | |
CSN306 | Durbanville | European olive | MT814024 | TreeBASE S26669, tree Tr125044 | |
CSN307 | Stellenbosch | European olive | MT813865 | TreeBASE S26669, tree Tr125044 | |
CSN321 | Riebeek-Kasteel | European olive | MT814025 | TreeBASE S26669, tree Tr125044 | |
CSN338 | Stellenbosch | Wild olive | Not available | Species specific PCR, assay of Lesuthu et al. (2019) | |
CSN343 | Stellenbosch | Wild olive | MT813866 | TreeBASE S26669, tree Tr125044 | |
CSN348 | Paarl | European olive | MT813867 | TreeBASE S26669, tree Tr125044 | |
CSN549 | Somerset West | European olive | MT814026 | TreeBASE S26669, tree Tr125044 | |
CSN550 | Somerset West | European olive | MT814027 | TreeBASE S26669, tree Tr125044 | |
CSN867 | Hermanus | European olive | MT813903 | TreeBASE S26669, tree Tr125044 | |
CSN866 | Hermanus | European olive | MT813902 | TreeBASE S26669, tree Tr125044 | |
PMM2076 | Stellenbosch | European olive | MT813998 | TreeBASE S26669, tree Tr125044 | |
PMM2079 | Stellenbosch | European olive | MT814001 | TreeBASE S26669, tree Tr125044 | |
PMM2080 | Stellenbosch | European olive | MT814002 | TreeBASE S26669, tree Tr125044 | |
PMM2081 | Paarl | European olive | MT814003 | TreeBASE S26669, tree Tr125044 | |
PMM2083 | Stellenbosch | European olive | MT814004 | TreeBASE S26669, tree Tr125044 | |
PMM2161 | Bonnievale | Wild olive | MT814011 | TreeBASE S26669, tree Tr125044 | |
Didymocyrtis banksiae | CSN1049 | Hermanus | European olive | MT813909 | TreeBASE S26669, tree Tr125042 |
CSN1050 | Hermanus | European olive | Not available | Morphological similarity to CSN1049 | |
CSN1065 | Wellington | Wild olive | MT813919 | TreeBASE S26669, tree Tr125042 | |
Didymosphaeria rubi-ulmifolii | CSN634 | Somerset West | European olive | MT813894 | TreeBASE S26669, tree Tr125047 |
CSN1150 | Paarl | Wild olive | MT813942 | TreeBASE S26669, tree Tr125047 | |
Didymosphaeria variabile | CSN618 | Riebeek-Kasteel | European olive | MT813884 | TreeBASE S26669, tree Tr125047 |
CSN1932 | Vredendal | European olive | MT813980 | TreeBASE S26669, tree Tr125047 | |
Diplodia seriata | ID0683 | Hermanus | European olive | MT813193 (EF), MT813986 (ITS) | TreeBASE S26669, tree Tr125045 |
PMM2093 | Paarl | European olive | MT814037 | TreeBASE S26669, tree Tr125045 | |
Eutypa lata | ID0305 | Ceres | European olive | Not available | Morphologically similar to ID0318 |
ID0318 | Ceres | Wild olive | MT813985 | TreeBASE S26669, tree Tr125046 | |
ID0319 | Ceres | Wild olive | Not available | Morphologically similar to ID0318 | |
PMM2905 | Riebeek-Kasteel | European olive | MT814012 | TreeBASE S26669, tree Tr125046 | |
PMM2907 | Durbanville | Wild olive | Not available | Morphologically similar to PMM2905 | |
PMM3064 | Stellenbosch | European olive | Not available | Morphologically similar to PMM3071 | |
PMM3066 | Stellenbosch | European olive | Not available | Morphologically similar to PMM3071 | |
PMM3067 | Stellenbosch | European olive | Not available | Morphologically similar to PMM3071 | |
PMM3068 | Hermanus | European olive | Not available | Morphologically similar to PMM3071 | |
PMM3069 | Hermanus | European olive | Not available | Morphologically similar to PMM3071 | |
PMM3070 | Hermanus | European olive | Not available | Morphologically similar to PMM3071 | |
PMM3071 | Hermanus | European olive | MT814013 | TreeBASE S26669, tree Tr125046 | |
Exophiala sideris | CSN1190 | Hermanus | European olive | MT813960 | TreeBASE S26669, tree Tr125030 |
Exophiala sp. CFJS-2015a | CSN1170 | Paarl | European olive | MT814031 | TreeBASE S26669, tree Tr125030 |
Exophiala sp. CFJS-2015b | CSN995 | Hermanus | European olive | MT813908 | TreeBASE S26669, tree Tr125030 |
Exophiala xenobiotica | CSN1930 | Vredendal | European olive | MT813978 | TreeBASE S26669, tree Tr125030 |
Fomitiporella sp. (Taxon 1) | CSN503 | Paarl | European olive | Not available | Morphologically similar to PMM2086 |
CSN505 | Paarl | European olive | Not available | Morphologically similar to PMM2086 | |
CSN518 | Paarl | European olive | Not available | Morphologically similar to PMM2086 | |
CSN944 | Hermanus | European olive | MT813904 | TreeBASE S26669, tree Tr125048 | |
CSN1936 | Vredendal | European olive | MT813982 | TreeBASE S26669, tree Tr125048 | |
PMM2086 | Paarl | European olive | MT814042 | TreeBASE S26669, tree Tr125048 | |
Geosmithia sp. CFJS-2015a | CSN158 | Calitzdorp | Wild olive | MT813861 | TreeBASE S26669, tree Tr125049 |
CSN159 | Calitzdorp | European olive | MT813862 | TreeBASE S26669, tree Tr125049 | |
PMM2037 | Paarl | European olive | MT813994 | TreeBASE S26669, tree Tr125049 | |
Helminthosporium asterinum | CSN1166 | Stellenbosch | European olive | MT813952 | BLAST – 97.13 %) ITS identity to Ellisembia asterinum CBS 203.35 AF073918 (98 %) coverage. No suitable reference sequences available for phylogenetic analysis. |
Herpotrichiellaceae sp. CFJS-2015a | CSN1211 | Durbanville | Wild olive | MT813965 | TreeBASE S26669, tree Tr125030 |
Heterophoma sp. | CSN1929 | Vredendal | European olive | MT813977 | TreeBASE S26669, tree Tr125050 |
Hysterium sp. CFJS-2015a | CSN1227 | Hermanus | European olive | MT813971 | TreeBASE S26669, tree Tr125038 |
Hysterium sp. CFJS-2015b | CSN1108 | Paarl | Wild olive | MT813937 | TreeBASE S26669, tree Tr125038 |
Jattaea sp. CFJS-2015a | CSN1152 | Stellenbosch | European olive | MT813943 | TreeBASE S26669, tree Tr125029 |
Kirschsteiniothelia sp. CFJS-2015a | CSN602 | Paarl | European olive | MT813880 | TreeBASE S26669, tree Tr125039 |
CSN604 | Wellington | Wild olive | MT813881 | TreeBASE S26669, tree Tr125039 | |
CSN605 | Paarl | European olive | MT813882 | TreeBASE S26669, tree Tr125039 | |
Lembosiniella sp. CFJS-2015a | CSN1210 | Hermanus | European olive | MT813964 | TreeBASE S26669, tree Tr125040 |
CSN1225 | Hermanus | European olive | MT813970 | TreeBASE S26669, tree Tr125040 | |
Leptosillia sp. CFJS-2015a | PMM2101 | Paarl | European olive | MT814010 | TreeBASE S26669, tree Tr125041 |
Lophiostoma cynaroidis | CSN1107 | Wellington | Wild olive | MT813936 | TreeBASE S26669, tree Tr125051 |
CSN1178 | Paarl | European olive | MT813958 | TreeBASE S26669, tree Tr125051 | |
Meyerozyma guilliermondii | CSN1219 | Hermanus | European olive | MT813966 | TreeBASE S26669, tree Tr125052 |
CSN1223 | Hermanus | European olive | MT813968 | TreeBASE S26669, tree Tr125052 | |
Mycocalicium victoriae | CSN1128 | Hermanus | European olive | MT813939 | TreeBASE S26669, tree Tr125053 |
CSN1129 | Somerset West | European olive | Not available | Morphological similarity to CSN1128 | |
CSN1130 | Hermanus | European olive | MT813940 | TreeBASE S26669, tree Tr125053 | |
CSN1131 | Hermanus | European olive | Not available | Morphological similarity to CSN1128 | |
CSN1194 | Hermanus | European olive | MT813961 | TreeBASE S26669, tree Tr125053 | |
Neocucurbitaria cava/juglandicola | CSN631 | Stellenbosch | European olive | MT813892 | TreeBASE S26669, tree Tr125054 |
Neocucurbitaria unguis-hominis | CSN629 | Paarl | European olive | MT813890 | TreeBASE S26669, tree Tr125054 |
Neodevriesia fraserae | CSN1169 | Somerset West | European olive | MT813955 | TreeBASE S26669, tree Tr125055 |
Neofusicoccum australe | ID0395 | Riebeek-Kasteel | European olive | MT274485, MT295262 | TreeBASE S26669, tree Tr125056 |
ID0403 | Stellenbosch | European olive | MT274487, MT295264 | TreeBASE S26669, tree Tr125056 | |
ID0493 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0498 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0499 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0500 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0507 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0508 | Durbanville | European olive | Not available | DNA fingerprinting, protocol of Alves et al. (2007) | |
ID0656 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0663 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0671 | Hermanus | European olive | Not available | DNA fingerprinting, protocol of Alves et al. (2007) | |
ID0672 | Hermanus | European olive | Not available | DNA fingerprinting, protocol of Alves et al. (2007) | |
ID0677 | Hermanus | European olive | Not available | DNA fingerprinting, protocol of Alves et al. (2007) | |
ID0678 | Hermanus | European olive | Not available | DNA fingerprinting, protocol of Alves et al. (2007) | |
ID0681 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
PMM2094 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
PMM2095 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
Neofusicoccum cryptoaustrale/stellenboschiana 3 | CSN179 | Strand | Wild olive | Not available | TreeBASE S26669, tree Tr125056 |
ID0416 | Stellenbosch | European olive | MT274489, MT295266 | TreeBASE S26669, tree Tr125056 | |
ID0489 | Durbanville | European olive | MT274491, MT295268 | TreeBASE S26669, tree Tr125056 | |
ID0490 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0491 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0492 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0494 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0496 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0658 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0661 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0664 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0665 | Hermanus | European olive | Not available | DNA fingerprinting, protocol of Alves et al. (2007) | |
ID0666 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0668 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0669 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0673 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0674 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0680 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0744 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0837 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
PMM2089 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
PMM2096 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
Neofusicoccum sp. 4 | ID0660 | Hermanus | European olive | MT274493, MT295270 | TreeBASE S26669, tree Tr125056 |
Neofusicoccum sp. 8 | ID0828 | Hermanus | European olive | MT274494, MT295271 | TreeBASE S26669, tree Tr125056 |
ID0847 | Hermanus | European olive | MT274495, MT295272 | TreeBASE S26669, tree Tr125056 | |
Neofusicoccum sp. PMM-2014a | PMM2097 | Paarl | European olive | MT814007 | TreeBASE S26669, tree Tr125056 |
PMM2098 | Paarl | European olive | MT814008 | TreeBASE S26669, tree Tr125056 | |
PMM2100 | Paarl | European olive | MT814009 | TreeBASE S26669, tree Tr125056 | |
Neofusicoccum sp. WvJ-2015a | CSN180 | Franschhoek | Wild olive | MT274479, MT295256 | TreeBASE S26669, tree Tr125056 |
ID0396 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
ID0402 | Stellenbosch | European olive | MT274486, MT295263 | TreeBASE S26669, tree Tr125056 | |
ID0417 | Stellenbosch | European olive | MT274490, MT295267 | TreeBASE S26669, tree Tr125056 | |
ID0495 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
PMM2090 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
PMM2091 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
PMM2092 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
PMM2099 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
Neofusicoccum vitifusiforme | CSN182 | Franschhoek | Wild olive | MT274497, MT295274 | TreeBASE S26669, tree Tr125056 |
ID0827 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125056 | |
Neophaeomoniella niveniae | CSN742 | Stellenbosch | Wild olive | See Table 1 | Fig. 3 |
CSN985 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN1916 | Klawer | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN1919 | Klawer | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
Neophaeomoniella zymoides | CSN743 | Stellenbosch | Wild olive | See Table 1 | Fig. 3 |
CSN986 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN1913 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
Nigrograna sp. CFJS-2015a | CSN591 | Stellenbosch | European olive | MT813879 | TreeBASE S26669, tree Tr125057 |
Nigrospora zimmermanii | CSN1157 | Riebeek-Kasteel | European olive | MT813945 | TreeBASE S26669, tree Tr125058 |
Parapyrenochaeta protearum | CSN1911 | Stellenbosch | European olive | MT813972 | TreeBASE S26669, tree Tr125059 |
Peniophora lycii | CSN371 | Stellenbosch | European olive | MT813868 | TreeBASE S26669, tree Tr125061 |
CSN509 | Stellenbosch | European olive | Not available | Morphologically similar to CSN371 | |
Phaeoacremonium africanum | CSN946 | Durbanville | European olive | KY906773 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 |
Phaeoacremonium minimum | PMM2073 | Stellenbosch | European olive | KY906895 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 |
Phaeoacremonium oleae | CSN403 | Paarl | Wild olive | KY906719 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 |
CSN413 | Wellington | Wild olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN703 | Stellenbosch | Wild olive | KY906751 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 | |
CSN720 | Wellington | Wild olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN721 | Wellington | Wild olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN945 | Durbanville | Wild olive | KY906771 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 | |
CSN1154 | Durbanville | Wild olive | Not available | TreeBASE S26669, tree Tr125062 | |
ID0231 | Ceres | Wild olive | Not available | TreeBASE S26669, tree Tr125062 | |
PMM1980 | Stellenbosch | Wild olive | Not available | TreeBASE S26669, tree Tr125062 | |
PMM1981 | Stellenbosch | Wild olive | KY906891 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 | |
PMM2440 | Bonnievale | Wild olive | KY906937 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 | |
Phaeoacremonium parasiticum | CSN418 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125062 |
CSN476 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN624 | Durbanville | European olive | KY906731 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 | |
Phaeoacremonium prunicola | ID0230 | Ceres | Wild olive | KY906817 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 |
Phaeoacremonium scolyti | CSN676 | Paarl | European olive | KY906743 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 |
CSN1193 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN1196 | Hermanus | European olive | KY906779 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 | |
CSN1199 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN1200 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN1201 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN1205 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN1206 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN1208 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN1212 | Stellenbosch | Wild olive | KY906781 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 | |
CSN1213 | Paarl | European olive | KY906783 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 | |
CSN1214 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN1215 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN1217 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125062 | |
CSN1218 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125062 | |
Phaeoacremonium spadicum | ID0208 | Ceres | Wild olive | KY906815 | TreeBASE S26669, tree Tr125062; Spies et al. 2018 |
Phaeoannellomyces elegans | CSN1921 | Klawer | Wild olive | MT814034 | TreeBASE S26669, tree Tr125030 |
Phialemoniopsis cornearis | CSN1175 | Somerset West | European olive | MT813956 | TreeBASE S26669, tree Tr125063 |
Phialemoniopsis ocularis | CSN1177 | Riebeek-Kasteel | European olive | MT813957 | TreeBASE S26669, tree Tr125063 |
CSN1183 | Durbanville | Wild olive | MT814033 | TreeBASE S26669, tree Tr125063 | |
CSN1224 | Hermanus | European olive | MT813969 | TreeBASE S26669, tree Tr125063 | |
Phialocephala oblonga | CSN630 | Stellenbosch | European olive | MT813891 | TreeBASE S26669, tree Tr125064 |
Phialocephala sp. CFJS-2015b | CSN1185 | Stellenbosch | European olive | MT813959 | TreeBASE S26669, tree Tr125064 |
Phlebia acerina | PMM2070 | Stellenbosch | European olive | MT813996 | TreeBASE S26669, tree Tr125065 |
Pleosporineae sp. CFJS-2015a | CSN650 | Riebeek-Kasteel | European olive | MT813898 | TreeBASE S26669, tree Tr125059 |
CSN1923 | Stellenbosch | European olive | MT814035 | TreeBASE S26669, tree Tr125059 | |
Pleurostoma richardsiae | CSN144 | Robertson | European olive | MT813859 | TreeBASE S26669, tree Tr125029 |
CSN145 | Robertson | European olive | MT813860 | TreeBASE S26669, tree Tr125029 | |
CSN493 | Paarl | European olive | MT813870 | TreeBASE S26669, tree Tr125029 | |
CSN495 | Paarl | Wild olive | Not available | Morphological characteristics | |
CSN496 | Paarl | European olive | MT813871 | TreeBASE S26669, tree Tr125029 | |
CSN500 | Durbanville | European olive | MT813872 | TreeBASE S26669, tree Tr125029 | |
CSN501 | Botrivier | European olive | MT813873 | TreeBASE S26669, tree Tr125029 | |
CSN514 | Paarl | European olive | MT813874 | TreeBASE S26669, tree Tr125029 | |
CSN515 | Stellenbosch | Wild olive | Not available | Morphological characteristics | |
CSN947 | Hermanus | European olive | MT813905 | TreeBASE S26669, tree Tr125029 | |
CSN1101 | Hermanus | European olive | MT813934 | TreeBASE S26669, tree Tr125029 | |
CSN1161 | Hermanus | European olive | MT813947 | TreeBASE S26669, tree Tr125029 | |
CSN1925 | Klawer | Wild olive | MT813974 | TreeBASE S26669, tree Tr125029 | |
PMM2011 | Stellenbosch | European olive | Not available | Morphological characteristics | |
PMM2012 | Paarl | European olive | Not available | Morphological characteristics | |
PMM2013 | Paarl | European olive | Not available | Morphological characteristics | |
Preussia africana | CSN626 | Riebeek-Kasteel | European olive | MT813888 | TreeBASE S26669, tree Tr125066 |
Preussia minima | CSN1111 | Riebeek-Kasteel | European olive | MT813938 | TreeBASE S26669, tree Tr125066 |
Pseudocamarosporium africanum | CSN1104 | Paarl | Wild olive | MT813935 | TreeBASE S26669, tree Tr125067 |
Pseudolophiostoma sp. CFJS-2015a | CSN1198 | Hermanus | European olive | MT813962 | TreeBASE S26669, tree Tr125051 |
Pseudophaeomoniella globosa | CSN18 | Franschhoek | Wild olive | See Table 1 | Fig. 3 |
CSN19 | Franschhoek | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN41 | Strand | Wild olive | See Table 1 | Fig. 3 | |
CSN183 | Calitzdorp | Wild olive | See Table 1 | Fig. 3 | |
CSN185 | Robertson | European olive | See Table 1 | Fig. 3 | |
CSN186 | Calitzdorp | European olive | See Table 1 | Fig. 3 | |
CSN294 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN299 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN304 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN305 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN310 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN314 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN315 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN319 | Stellenbosch | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN325 | Stellenbosch | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN329 | Stellenbosch | Wild olive | See Table 1 | Fig. 3 | |
CSN334 | Paarl | Wild olive | See Table 1 | Fig. 3 | |
CSN339 | Paarl | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN344 | Stellenbosch | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN349 | Paarl | European olive | See Table 1 | Fig. 3 | |
CSN375 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN377 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN381 | Wellington | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN382 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN385 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN386 | Wellington | Wild olive | See Table 1 | Fig. 3 | |
CSN390 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN391 | Wellington | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN395 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN396 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN397 | Riebeek-Kasteel | European olive | Not available | Species specific PCR (Van Dyk 2020) | |
CSN400 | Stellenbosch | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN401 | Wellington | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN405 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN409 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN410 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN412 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN424 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN427 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN435 | Riebeek-Kasteel | European olive | See Table 1 | Fig. 3 | |
CSN441 | Stellenbosch | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN446 | Stellenbosch | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN448 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN451 | Stellenbosch | European olive | See Table 1 | Fig. 3 | |
CSN463 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN726 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN727 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN728 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN729 | Paarl | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN730 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN731 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN733 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN735 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN736 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN737 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN738 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN739 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN746 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN750 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN751 | Wellington | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN752 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN753 | Stellenbosch | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN754 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN755 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN756 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN757 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN759 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN765 | Wellington | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN766 | Wellington | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN769 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN771 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN788 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN791 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN792 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN799 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN800 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN802 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN803 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN804 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN806 | Durbanville | Wild olive | See Table 1 | Fig. 3 | |
CSN808 | Durbanville | European olive | See Table 1 | Fig. 3 | |
CSN816 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN818 | Durbanville | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN824 | Somerset West | European olive | See Table 1 | Fig. 3 | |
CSN825 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN831 | Riebeek-Kasteel | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN834 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN835 | Durbanville | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN838 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN950 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN952 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN954 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN955 | Wellington | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN956 | Wellington | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN960 | Hermanus | European olive | See Table 1 | Fig. 3 | |
CSN961 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN962 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN965 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN966 | Hermanus | European olive | Not available | Species specific PCR (Van Dyk 2020) | |
CSN968 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN971 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN972 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN973 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN976 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN979 | Somerset West | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN982 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN991 | Hermanus | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN1900 | Piketberg | European olive | Not available | Species specific PCR (Van Dyk 2020) | |
CSN1914 | Klawer | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
CSN1915 | Klawer | Wild olive | Not available | Species specific PCR (Van Dyk 2020) | |
CSN1920 | Lutzville | Wild olive | Not available | Species specific PCR (Van Dyk 2020) | |
ID0250 | Ceres | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
ID0251 | Ceres | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
ID0253 | Ceres | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
ID0255 | Ceres | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
ID0256 | Ceres | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
ID0258 | Ceres | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
ID0263 | Ceres | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
ID0264 | Ceres | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
PMM1192 | Vredendal | European olive | See Table 1 | Fig. 3 | |
PMM2017 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
PMM2018 | Paarl | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
PMM2044 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
PMM2047 | Paarl | European olive | Not available | Morphological similarity to PMM2044 | |
PMM2052 | Paarl | European olive | Not available | Morphological similarity to PMM2044 | |
PMM2057 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
PMM2060 | Stellenbosch | European olive | Not available | TreeBASE S26669, tree Tr125034 | |
PMM2061 | Stellenbosch | European olive | Not available | Species specific PCR (Van Dyk 2020) | |
PMM2484 | Bonnievale | Wild olive | See Table 1 | Fig. 3 | |
PMM2485 | Bonnievale | Wild olive | Not available | TreeBASE S26669, tree Tr125034 | |
Punctularia atropurpurascens | CSN1060 | Durbanville | Wild olive | MT813915 | TreeBASE S26669, tree Tr125068 |
CSN1061 | Wellington | Wild olive | MT813916 | TreeBASE S26669, tree Tr125068 | |
Sarocladium strictum | CSN1202 | Hermanus | European olive | MT813963 | TreeBASE S26669, tree Tr125069 |
CSN1220 | Hermanus | European olive | MT813967 | TreeBASE S26669, tree Tr125069 | |
Schizophyllum commune | CSN336 | Paarl | European olive | Not available | Morphological similarity to PMM2088. |
CSN528 | Paarl | European olive | Not available | Morphological similarity to PMM2088. | |
CSN1160 | Hermanus | European olive | MT813946 | TreeBASE S26669, tree Tr125070 | |
PMM2087 | Stellenbosch | European olive | MT814005 | TreeBASE S26669, tree Tr125070 | |
PMM2088 | Paarl | European olive | MT814006 | TreeBASE S26669, tree Tr125070 | |
Symbiotaphrina microtheca | CSN615 | Stellenbosch | European olive | MT813883 | TreeBASE S26669, tree Tr125071 |
CSN1163 | Hermanus | European olive | MT813949 | TreeBASE S26669, tree Tr125071 | |
CSN1164 | Hermanus | European olive | MT813950 | TreeBASE S26669, tree Tr125071 | |
CSN1165 | Hermanus | European olive | MT813951 | TreeBASE S26669, tree Tr125071 | |
Teichospora sp. CFJS-2015a | CSN953 | Durbanville | Wild olive | MT813906 | TreeBASE S26669, tree Tr125051 |
CSN1083 | Stellenbosch | European olive | MT813927 | TreeBASE S26669, tree Tr125051 | |
CSN1084 | Durbanville | Wild olive | MT813928 | TreeBASE S26669, tree Tr125051 | |
CSN1085 | Stellenbosch | European olive | MT813929 | TreeBASE S26669, tree Tr125051 | |
CSN1086 | Paarl | European olive | MT813930 | TreeBASE S26669, tree Tr125051 | |
CSN1087 | Paarl | Wild olive | MT813931 | TreeBASE S26669, tree Tr125051 | |
CSN1088 | Paarl | European olive | MT813932 | TreeBASE S26669, tree Tr125051 | |
Torula ficus | PMM2032 | Stellenbosch | European olive | MT813991 | TreeBASE S26669, tree Tr125072 |
Trametes versicolor | CSN1058 | Stellenbosch | European olive | MT813914 | TreeBASE S26669, tree Tr125073 |
ID0244 | Ceres | European olive | MT813984 | TreeBASE S26669, tree Tr125073 | |
Tympanis sp. CFJS-2015a | CSN1093 | Hermanus | European olive | MT813933 | TreeBASE S26669, tree Tr125074 |
Unknown – aff. Anthopsis catenata | CSN406 | Paarl | European olive | MT813869 | BLAST – 81.89 % ITS identity to Anthopsis catenata CBS 492.81 NR_159623 (87 % coverage). |
Unknown – aff. Phaeomoniellales | CSN783 | Riebeek-Kasteel | European olive | MT813672 (18S), MT814041 (ITS) | Partial 18S BLAST (404bp) – 94.43 % identity to Pseudophaeomoniella oleicola CBS 139192 KP411807 (88 % coverage). ITS BLAST – No significant similarity found. |
Unknown – Pleosporales sp. | CSN1927 | Vredendal | European olive | MT813976 | TreeBASE S26669, tree Tr125075 |
Unknown – Pleosporales sp. | CSN1933 | Vredendal | European olive | MT813981 | TreeBASE S26669, tree Tr125075 |
Unknown – Pleosporales sp. | CSN1926 | Vredendal | European olive | MT813975 | TreeBASE S26669, tree Tr125075 |
Unknown – putative Bezerromycetales sp. | CSN1931 | Klawer | Wild olive | MT813979 | TreeBASE S26669, tree Tr125076 |
Unknown – putative Debaryomycetaceae sp. | CSN781 | Stellenbosch | European olive | MT813901 | TreeBASE S26669, tree Tr125052 |
Unknown – putative Verrucariaceae sp. | CSN741 | Paarl | European olive | MT813900 | TreeBASE S26669, tree Tr125060 |
Vredendaliella oleae | PMM1193 | Vredendal | European olive | See Table 1 | Fig. 3 |
Xenocylindrosporium margaritarum | CSN1179 | Paarl | European olive | See Table 1 | Fig. 3 |
CSN1216 | Somerset West | European olive | See Table 1 | Fig. 3 | |
CSN1917 | Klawer | Wild olive | See Table 1 | Fig. 3 | |
Xenocylindrosporium sp. CFJS-2015c | CSN1180 | Paarl | European olive | See Table 1 | Fig. 3 |
CSN1184 | Stellenbosch | European olive | See Table 1 | Fig. 3 | |
CSN1203 | Hermanus | European olive | See Table 1 | Fig. 3 | |
Xenocylindrosporium sp. CFJS-2015e | CSN1222 | Hermanus | European olive | See Table 1 | Fig. 3 |
Xenocylindrosporium sp. CFJS-2015f | CSN1191 | Hermanus | European olive | See Table 1 | Fig. 3 |
Xenocylindrosporium sp. CFJS-2015g | CSN1174 | Somerset-West | European olive | See Table 1 | Fig. 3 |
Xylonomycetes sp. CFJS-2015a | CSN958 | Hermanus | European olive | MT813907 | TreeBASE S26669, tree Tr125071 |
1CSN: collection of Chris Spies at ARC-Nietvoorbij, Stellenbosch, South Africa; ID: collection of Ihan du Plessis at ARC-Nietvoorbij, Stellenbosch, South Africa; PMM: collection of Providence Moyo at the University of Stellenbosch, Department of Plant Pathology, Stellenbosch, South Africa.
2Phylogenies are referred to by figure reference or TreeBASE accession numbers. Details of other methods of identification are provided.
3In the current investigation, these two species could not be distinguished using ITS, TEF1α, and TUB2 sequence data alone or in combination.
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Data
Data behind the article
This data has been text mined from the article, or deposited into data resources.
BioStudies: supplemental material and supporting data
Nucleotide Sequences (Showing 176 of 176)
- (2 citations) ENA - AY254052
- (2 citations) ENA - AY254051
- (1 citation) ENA - MH999539
- (1 citation) ENA - GQ154599
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- (1 citation) ENA - MH999537
- (1 citation) ENA - KF764636
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- (1 citation) ENA - MT791057
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- (1 citation) ENA - KR260451
- (1 citation) ENA - MT791055
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- (1 citation) ENA - KT804064
- (1 citation) ENA - KR260453
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- (1 citation) ENA - KR260455
- (1 citation) ENA - MT791059
- (1 citation) ENA - GU345749
- (1 citation) ENA - KR260454
- (1 citation) ENA - MT791053
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- (1 citation) ENA - JQ044435
- (1 citation) ENA - MT787409
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- (1 citation) ENA - MW017334
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- (1 citation) ENA - MK070469
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- (1 citation) ENA - KY173487
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- (1 citation) ENA - KP635974
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- (1 citation) ENA - KR476731
- (1 citation) ENA - AF253968
- (1 citation) ENA - GU332515
- (1 citation) ENA - KP635970
- (1 citation) ENA - DQ270253
- (1 citation) ENA - MW017340
- (1 citation) ENA - KF764683
- (1 citation) ENA - MK070473
- (1 citation) ENA - MK070475
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- (1 citation) ENA - FJ372408
- (1 citation) ENA - MK070477
- (1 citation) ENA - MN861685
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- (1 citation) ENA - MN861680
- (1 citation) ENA - MT787418
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- (1 citation) ENA - MT787413
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- (1 citation) ENA - MT787412
- (1 citation) ENA - DQ329020
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- (1 citation) ENA - MT787411
- (1 citation) ENA - MT787410
- (1 citation) ENA - MT787377
- (1 citation) ENA - MT787376
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- (1 citation) ENA - MT787373
- (1 citation) ENA - MT787383
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- (1 citation) ENA - MN232957
- (1 citation) ENA - MT787381
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- (1 citation) ENA - MT797854
- (1 citation) ENA - MT797853
- (1 citation) ENA - MT797855
- (1 citation) ENA - MT797850
- (1 citation) ENA - MT791071
- (1 citation) ENA - MN861679
- (1 citation) ENA - MT791072
- (1 citation) ENA - MT797852
- (1 citation) ENA - MN861678
- (1 citation) ENA - MN861677
- (1 citation) ENA - MT797851
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- (1 citation) ENA - MN861676
- (1 citation) ENA - MT791075
- (1 citation) ENA - MT791076
- (1 citation) ENA - MT791073
- (1 citation) ENA - MT791074
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- (1 citation) ENA - MH861028
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- (1 citation) ENA - JQ044454
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- (1 citation) ENA - MT787392
- (1 citation) ENA - MT787391
- (1 citation) ENA - MT787390
- (1 citation) ENA - KP992094
- (1 citation) ENA - KR476766
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RefSeq - NCBI Reference Sequence Database (Showing 14 of 14)
- (1 citation) RefSeq - NR_138001
- (1 citation) RefSeq - NR_132824
- (1 citation) RefSeq - NR_155612
- (1 citation) RefSeq - NR_132005
- (1 citation) RefSeq - NR_137711
- (1 citation) RefSeq - NR_132841
- (1 citation) RefSeq - NR_137965
- (1 citation) RefSeq - NR_137966
- (1 citation) RefSeq - NG_042750
- (1 citation) RefSeq - NR_132004
- (1 citation) RefSeq - NR_111823
- (1 citation) RefSeq - NR_132003
- (1 citation) RefSeq - NR_161148
- (1 citation) RefSeq - NG_066265
Show less
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