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Article

A New Mitochondrial Genome of Sogatella furcifera (Horváth) (Hemiptera: Delphacidae) and Mitogenome-Wide Investigation on Polymorphisms

by
Jongsun Park
1,*,
Hong Xi
1,
Jonghyun Park
1 and
Bo Yoon Seo
2,*
1
InfoBoss Research Center, InfoBoss Inc., 301 Room, 670, Seolleung-ro, Gangnam-gu, Seoul 06088, Korea
2
Crop Protection Division, National Institute of Agricultural Sciences, RDA, Wanju 55365, Korea
*
Authors to whom correspondence should be addressed.
Insects 2021, 12(12), 1066; https://doi.org/10.3390/insects12121066
Submission received: 28 August 2021 / Revised: 16 November 2021 / Accepted: 25 November 2021 / Published: 27 November 2021
(This article belongs to the Section Insect Molecular Biology and Genomics)
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Abstract

:

Simple Summary

We completed one mitogenome of white-backed planthopper (WBPH), Sogatella furcifera (Horváth), with finding heteroplasmy phenomenon confirmed by PCR reaction and Sanger sequencing method. This heteroplasmy was not observed in WBPHs (n = 24) collected from the fields, suggesting that it may be uncommon in fields. We also analyzed single nucleotide polymorphisms, insertion and deletions, and simple sequence repeats among three currently available WBPH mitogenomes of Korea and China, suggesting that identified intraspecific variations could be potential candidates for developing markers to distinguish geographical populations of WBPH including Korean and Chinese. Phylogenetic analysis of 32 mitogenomes of Delphacidae including the three WBPH mitogenomes suggested that Delphacinae seems to be monophyletic and Sogatella species including WBPH are clearly formed as one clade.

Abstract

White-backed planthopper (WBPH), Sogatella furcifera (Horváth), is one of the major sap-sucking rice pests in East Asia. We have determined a new complete mitochondrial genome of WBPH collected in the Korean peninsula using NGS technology. Its length and GC percentages are 16,613 bp and 23.8%, respectively. We observed one polymorphic site, a non-synonymous change, in the COX3 gene with confirmation heteroplasmy phenomenon within individuals of WBPH by PCR amplification and Sanger sequencing, the first report in this species. In addition, this heteroplasmy was not observed in wild WBPH populations, suggesting that it may be uncommon in fields. We analyzed single nucleotide polymorphisms, insertion, and deletions, and simple sequence repeats among the three WBPH mitogenomes from Korea and China and found diverse intraspecific variations, which could be potential candidates for developing markers to distinguish geographical populations. Phylogenetic analysis of 32 mitogenomes of Delphacidae including the three WBPH mitogenomes suggested that Delphacinae seems to be monophyletic and Sogatella species including WBPH are clearly formed as one clade. In the future, it is expected that complete mitogenomes of individuals of geographically dispersed WBPH populations will be used for further population genetic studies to understand the migration pathway of WBPH.

1. Introduction

Sogatella furcifera (Horváth), commonly called the white-backed planthopper (WBPH), is an important rice pest species in East Asian rice fields [1,2]. It has usually migrated from the subtropic to temperate regions. For example, they migrate from China to Korea almost every year [1], resulting in this species being listed on the National Species List of Korea [3]. It damages rice plants by feeding directly, causing a decreased filling percentage of kernels and kernel weights [4], and hopper burn is a characteristic symptom of WBPH [5]. Due to the economic importance of this species in rice-cultivating areas [6], whole genome [7], and complete mitochondrial genomes [8] were successfully sequenced and analyzed. These genomic resources of WBPH, which are already available for in-depth analyses, provide a favorable environment for a detailed investigation of its mitochondrial genomes. Because of the regular migration of WBPH from China to Korea, identification of the origin of WBPH has become an important issue for controlling this pest [9,10,11]. One easy way to identify this is by utilizing molecular markers, including mitochondrial genes [12,13,14,15,16]. For example, the investigation of intraspecific variations in the mitochondrial genome of Laodelphax striatellus (Fallén) along with the samples distributed in China [17] demonstrated that the two major populations of L. striatellus, haplotypes A and B [17].
Next-generation sequencing (NGS) technologies [18,19,20] together with genome assembly programs based on NGS short reads [21,22,23,24,25] have increased the number of sequenced insect mitochondrial genomes. The number of available insect mitochondrial genomes was 6427 as of May 2021, according to the GenomeArchive® [26]. It is more than 48 times the number of insect mitochondrial genomes in 2009 (132 insect complete or near-complete mitochondrial genomes) [27]. In addition, the number of representative mitochondrial genome sequences that NCBI has curated is 2441, indicating that 2441 distinct insect species cover one or more mitochondrial genomes.
Because of the short length of NGS raw reads, especially those generated by the Illumina HiSeq platform (36 bp–151 bp) [28], the minimum depth for assembly is relatively high, for example, average 30× coverage for human genome resequencing [29], in comparison to that of the Sanger sequencing method: 6×–10× depth for de novo assembly [30,31]. Interestingly, this high coverage of NGS raw reads provides a deep profile of each base of the assembled mitochondrial genomes [32,33,34,35,36,37,38], usually because the amount of mitochondrial genomic DNA in a cell is much higher than that of the main chromosomes. This deep profile can provide the polymorphic bases that display more than one nucleotide in a specific position of the mitochondrial genome. Once these bases demonstrate that alternative nucleotides show a higher proportion than the base calling error rate, they can be potential polymorphic sites or misassemble areas.
The mitochondrial genome can be highly polymorphic among individuals even in the same species but is usually homogeneous within one individual in insects because it is inherited from the mother’s side [39]. However, different types of mitochondrial genomes in one individual, called mitochondrial heteroplasmy [40], can be found in unusual cases. Interestingly, this mitochondrial heteroplasmy has been reported in insect mitochondrial genomes, including Drosophila mauritiana Tsacas & David [41,42], bark weevils [43], Cimex lectularius Linnaeus [44], and Aedes aegypti (Linnaeus in Hasselquist) [45]. This indicates that many insect species may present with mitochondrial heteroplasmy. However, multiple individuals of small insects including planthoppers, are usually required to extract sufficient genomic DNA for NGS sequencing. Consequently, even though the sample does not exhibit heteroplasmy, the extracted DNA appears to demonstrate heteroplasmy because the DNA sample was derived from multiple individuals, with different sequences of the mitochondrial genome. This indicates that the NGS of small insects has the potential to exhibit a ‘virtual’ heteroplasmy problem. In this case, cross-confirmation of the actual nucleotide sequence by the Sanger sequencing method is required to investigate the mitogenome-wide polymorphism.
Here, we report a new WBPH mitochondrial genome and suggest the phenomenon of mitochondrial heteroplasmy from the assembled mitogenome of a WBPH sample consisting of multiple individuals. We confirmed this heteroplasmy phenomenon in the WBPH mitochondrial genome by comparing sequences of PCR products obtained from each individual sample using the Sanger sequencing method. In addition, we conducted a comparative analysis of WBPH mitogenomes to understand their intraspecific variations as well as simple sequence repeats (SSRs) to prepare the fundamental data to develop molecular markers to distinguish geographical populations of WBPH and to track its region-of-origin of migration. Finally, we carried out a phylogenetic analysis based on the complete mitogenomes of the family Delphacidae available and compared with the previous phylogenetic studies based on several marker sequences [46] to evaluate a newly assembled WBPH mitogenome data in this study. It provides the clear taxonomic relationship between WBPH captured in Korea and 30 species of Delphacidae and one species of Cixiidae.

2. Materials and Methods

2.1. DNA Extraction of the WBPH Samples

We extracted genomic DNA from a total of 20 WBPH individuals of the Taean population of WBPHs (named as WBPHTA) using the CTAB-based DNA extraction method (iNtRON biotechnology, Inc., Seoungnam-si, Korea) for next-generation sequencing. Each genomic DNA of ten WBPH individuals in WBPHTA and 24 WBPH individuals in two wild WBPH populations was additionally extracted and used to determine nucleotide sequences in a polymorphic site of the COX3 gene through Sanger sequencing. WBPHTA was captured at paddy fields (N 36°38′, E 126°18′) in Taean-gun in the Republic of Korea in 2006 and has been kept with rice seedlings in the insectary [25 ± 2 °C, 60 ± 5% RH, 14 (L): 10 (D)] of National Institute of Agricultural Sciences in Korea. The two wild populations, named as WBPHHD and WBPHBS, were sampled at paddy fields in Hadong-gun (N 34°58′20″, E 127°50′57″) and Boseong-gun (N 34°50′28″, E 127°16′36″), respectively, in the Republic of Korea on 19 July 2021.

2.2. Genome Sequencing and De Novo Assembly of WBPH Mitogenome

Genome sequencing was performed using HiSeqX at Macrogen Inc., Seoul, Korea from extracted DNA of the WBPH sample. De novo assembly and confirmation were done by Velvet v1.2.10 [21] after filtering raw reads using Trimmomatic v0.33 [47] with default parameters. The assembled mitochondrial genome sequence was confirmed with BWA v0.7.17 [48] (alignment of raw reads against the assembled sequence) and SAMtools v1.9 (tview mode for a manual check of each base) [49]. All bioinformatic processes were conducted under the environment of the Genome Information System (GeIS; http://geis.infoboss.co.kr/; 24 November 2021) which have been utilized in the various genomic studies [50,51,52,53].

2.3. Annotation of WBPH Mitogenome

Geneious Prime® v2020.2.4 (Biomatters Ltd., Auckland, New Zealand) was used to annotate mitochondrial genome based on the previously sequenced mitogenome of WBPH (NC_021417) [8] with ARWEN [54] for annotating tRNAs.

2.4. Verification of Polymorphic Sites on the WBPH Mitogenome Using PCR and Sanger Sequencing Methods

To verify the sequence of one polymorphic site (A/T4667) in the whole WBPH mitogenome, we designed a PCR primer set, Sofur-mt4218F (5′-ACA CTA ACC TAA TAT TTG CC-3′) and Sofur-mt4945R (5′-GAT GCT CCT GAT CTT AAT AA-3′). PCR amplification of each genomic DNA for ten WBPH individuals of WBPHTA, eight individuals of WBPHHD, and 16 individuals of WBPHBS was conducted with PrimeSTAR GXL DNA polymerase (Takara Korea Biomedical Inc., Seoul, Korea) by following 30 cycles of 10 s at 98 °C, 15 s at 50 °C, and 1 min at 68 °C. Sager sequencing of PCR products was carried out by the DNA sequencing service of Macrogen Inc. Korea using ABI 3730xl System (Thermo Fisher Scientific, MA, USA).

2.5. Prediction of Three-Dimensional Structure of COX3 of WBPH Mitogenome

To predict the three-dimensional structure of COX3, Swiss-Model (https://swissmodel.expasy.org/; 24 November 2021) [55] was used with the amino acid sequence of COX3. ‘Build Mode’ was used for constructing two types of COX3 amino acids caused by the heteroplasmy we identified in this study. The figure of the three-dimensional structure was also drawn by the web interface of Swiss-Model directly.

2.6. Identification of Intraspecific Variations of WBPH Mitogenomes

Pair-wise sequence alignments among complete mitogenome of WBPH including the mitogenome sequenced in this study were conducted by MAFFT v7.450 [56] with the default option. Identifying intraspecific variations, SNPs and INDELs, on the WBPH mitogenomes was conducted using the function, ‘Find variations/SNPs,’ implemented in the Geneious Prime® v2020.2.4 (Biomatters Ltd., Auckland, New Zealand), which has been utilized in the previous insect mitochondrial genome studies [37,57,58,59,60,61,62,63,64]. When the number of INDELs was calculated, continuous INDEL bases were considered one INDEL region.

2.7. Identification of Simple Sequence Repeats on the WBPH Mitogenomes

Simple sequence repeats (SSRs) were identified on the mitogenome sequence using the pipeline of the SSR database (SSRDB; http://ssrdb.infoboss.co.kr/; 24 November 2021) which has been utilized in the previous studies [65,66,67,68,69,70]. Based on the conventional definition of an SSR on the organelle genome, monoSSR (1 bp) to hexaSSR (6 bp), the total length of SSRs on the chloroplast genome exceeds 10 bp. We used the criteria as follows: the monoSSR (unit sequence length of 1 bp) to hexaSSR (6 bp) are used as normal SSRs, and heptaSSR (7 bp) to decaSSR (10 bp) are defined as extended SSRs. Among the normal SSRs, pentaSSRs (5 bp) and hexaSSRs (6 bp) are classified as potential SSRs.

2.8. Comparison of SSRs Identified from the WBPH Mitogenomes

SSRs identified from the three WBPH mitogenomes were compared based on their flanking sequences under the environment of the SSRDB (http://ssrdb.infoboss.co.kr/; 24 November 2021) to identify intraspecific variations of SSRs. The pipeline of the SSR comparison implemented in the SSRDB used in various organelle genome studies [65,68,69,70] was used with the following conditions: a cut-off e-value of 1 × 10−10 and a maximum flanking sequence for the comparison of 60 bp.

2.9. Construction of Phylogenetic Trees

The 33 mitogenomes including 32 representative mitogenomes (30 species) selected for each species in the Delphacidae family and one outgroup mitogenome of Haplaxius crudus (Van Duzee) in the Cixiidae family [46] were aligned without control region by MAFFT v7.450 [56], and alignment quality was checked manually. The maximum likelihood (ML) tree was reconstructed in IQ-TREE v1.6.6 [71]. In the ML analysis, a heuristic search was used with nearest-neighbor interchange (NNI) branch swapping, TVM + F + R4 model, and uniform rates among sites suggested by the model finder implemented in IQ-TREE. All other options used the default settings. Bootstrap analyses with 1000 pseudoreplicates were conducted with the same options. The posterior probability of each node was estimated by Bayesian inference (BI) using the MrBayes v3.2.6 [72] plug-in implemented in Geneious Prime®2020.2.4 (Biomatters Ltd., Auckland, New Zealand). The HKY85 model with gamma rates was used as a molecular model. A Markov chain Monte Carlo algorithm was employed for 1,100,000 generations, sampling trees every 200 generations, with four chains running simultaneously. Trees from the first 100,000 generations were discarded as burn-in.

3. Results and Discussions

3.1. Complete Mitochondrial Genome of S. furcifera

In this study, we present the complete mitochondrial genome of S. furcifera (WBPHTA; GenBank accession number: MK907866) with a length of 16,613 bp, containing 13 protein-coding genes (PCGs), 22 transfer RNAs (tRNAs), and 2 ribosomal RNAs (rRNAs) (Supplementary Table S1 and Figure 1), which is a typical configuration of insect mitochondrial genomes [73,74]. It is similar to one of the mitogenomes previously sequenced (WBPHHN; GenBank accession number: NC_021417; 16,612 bp; Table 1). The GC percentage of the WBPHTA mitogenome was 23.8%, which is the same as the previously sequenced WBPH mitogenomes (WBPHHN and WBPHYN; Table 1).
The AT-rich region, considered as a putative control region of the WBPHTA mitogenome, is 2219 bp long, which is the shortest length among the three WBPH mitogenomes (Table 1). The variations found in a putative control region mostly contributed to the length difference of WBPH mitogenomes (see the section, Intraspecific mitochondrial variations compared with the previously sequenced WBPH mitogenomes). Usually, variations of this putative control region are larger than those in the remaining regions [65], therefore, it can be utilized as a good genetic marker [75]. The GC-skew and AT-skew of the WBPHTA mitogenome are calculated as −0.14163 and 0.094715, respectively, similar to those of the other two WBPH mitogenomes (Table 1).
The length variations of complete mitogenomes of two planthopper species, the brown planthopper (BPH; Nilaparvata lugens (Stål)) [57,60,76,77,78] and the small brown planthopper (SBPH; L. striatellus) [63,77,79], were investigated (Figure 2A). Interestingly, the length variations of SBPH and BPH complete mitogenomes were approximately 1.5 kb and 3 kb, respectively, different from that of WBPH (i.e., less than 100 bp; Figure 2A). One SBPH (GenBank accession number: MW732715; unpublished) and five BPH complete mitogenomes [57,60,76,77,78] were significantly shorter than those of the remaining mitogenomes, due to the short length of the control region, or lack of this region. We speculate that these six mitogenomes might lack the control region, even though they were labeled as complete mitogenomes, because of difficulties of assembly. After removing these six short complete mitogenomes, SBPH exhibits the largest variations because of the large number (86) of complete mitogenomes [63,77,79], while the remaining two species exhibited a small range of length variations (Figure 2B), indicating that length variations of planthoppers can be affected by the number of mitogenome sequences obtained from individuals of various geographical regions.

3.2. Identification and Verification of the Polymorphic Site Found from the WBPH Mitogenome

During the base confirmation process of the assembled WBPH mitogenome, we found that one base of COX3 at 4667th starting from tRNA-Ile on the mitogenome, presented A and T together (Figure 3A). The ratio of A to T was close to 1:1 (Figure 3A), indicating that this site may have two different bases. In addition, sequencing depth around the region of 4667th nucleotide displayed around 19,000× depth without any duplication signal in this region (Figure 3B). This phenomenon can be explained by the fact that 20 WBPH individuals were used for extracting DNA (see Materials and Methods).
To confirm whether this polymorphic site contains both bases, we amplified the region around this site of the ten additional individuals (SF1 to SF10) by PCR and sequenced the PCR products using the Sanger sequencing method. We obtained the sequencing results from nine out of ten individuals (Figure 3B), resulting in five out of nine individuals, SF1, SF2, SF3, SF4, and SF6, presenting the polymorphic base, A and T, simultaneously within one individual (Figure 3B). Because of this polymorphic base, base calling results at this site from the five individuals were not consistent (Figure 3B). This result is different from what we expected, namely, that heterogeneous haplotypes from multiple individuals can cause a ‘virtual’ heteroplasmy phenomenon based on NGS results. However, there was a real heteroplasmy phenomenon in WBPH individuals, and this is the first report of heteroplasmy in the mitochondrial genome of a species in the family Delphacidae.
Because this heteroplasmy phenomenon was only observed in WBPH individuals from WBPHTA, a breeding line, has been established and reared in the insectary since 2006, it was necessary to evaluate whether this heteroplasmy in the WBPH mitogenome is also common in wild populations or not. A 4667th nucleotide sequence of COX3 from a total of 24 individuals of the two Korean wild WBPH populations, WBPHHD and WBPHBS, was investigated using PCR and the Sanger sequencing method. In the results, there was no heteroplasmy phenomenon and single nucleotide polymorphism (SNP; only A) at the 4667th of the WBPH mitogenome. It suggests that the heteroplasmy and SNP of WBPHTA mitogenome might be uncommon in the wild WBPH populations in fields. The heteroplasmy of WBPHTA mitogenome would be associated with continuous pressures from the inbreeding environment in the laboratory. It is remained to study whether this heteroplasmy phenomenon of WBPH is artificially created through continuous insect rearing indoors.
An amino acid substitution from lysine (L) to phenylalanine (F) in COX3 was deduced by changing A to T at the 4667th position. Moreover, there was one HexaSSR, H0000007 (Supplementary Table S2), which covered this polymorphic site. Once it changes from A to T, the SSR disappears. To evaluate the effectiveness of the three-dimensional structure of COX3 of non-synonymous SNP, we build the two models using the SWISS-MODEL [55] based on the translated amino acids of the two COX3 genes. The three-dimensional structure of COX3 of WBPH exhibited the structure of the seven alpha helixes (Figure 4), which is the same as the three-dimensional structure of the template sequence (2occ.1) with different spatial configurations. The amino acid at the 49th position of COX3 in both forms did not affect their alpha-helix structure (See red parts in Figure 4A,B), indicating that this non-synonymous mutation from heteroplasmy may not affect three-dimensional structure severely.
The heteroplasmy in the mitogenome has been found in various insect and mite species, including the bed bug (Cimex lectularius Linnaeus, Hemiptera:Cimicidae) [80], honeybee (Apis mellifera Linnaeus, Hymenoptera:Apidae) [81], a neotropical ant species (Ectatomma ruidum (Roger), Formicidae:Ectatomminae) [82], Anapodisma miramae Dovnar-Zapolskij (Orthoptera:Acrididae) [83], Tetrodontophora bielanensis (Waga) (Poduromorpha:Onychiuridae) [84], and Drosophila melanogaster Meigen (Diptera:Drosophilidae) and is caused by paternal mitochondrial DNA leakage [85,86]. It has been found that the heteroplasmy phenomenon in the mitogenome can be involved in biological functions, including pesticide resistance [87,88,89,90] and xenobiotics detoxification [91]. Taken together, our finding suggests that further investigation is needed to determine whether this mitochondrial heteroplasmy in WBPH has biological meanings, such as its physiological mechanism. Moreover, once insect mitogenomes assembled by NGS raw reads displayed any heterogeneous bases, they have to be validated using the other experimental methods whether these bases can be candidates of real heteroplasmy or not.

3.3. Intraspecific Mitochondrial Variations Compared with the Previously Sequenced WBPH Mitogenomes

Based on three pair-wise alignments of WBPH mitogenomes, 21 SNPs and four insertions and deletion (INDEL) regions (9 bp in total) and six SNPs and five INDEL regions (49 bp in total) against WBPHHN and WBPHYN mitogenomes were identified (Figure 5A). The longest INDEL found between the WBPHYN and WBPHTA mitogenomes were 42 bp in length in the control region. The control region is the most variable region in insect mitogenomes [65,75,92], which can explain the INDEL identified in the control region. In addition, 14 SNPs and six INDEL regions (50 bp in total) were also found between the WBPHHN and WBPHYN mitogenomes, displaying the same 42-bp INDEL between the two mitogenomes (Figure 5B).
Thirteen of 21 SNPs (61.90%) between the WBPHTA and WBPHHN mitogenomes, six of six SNPs (100.00%) between the WBPHTA and WBPHYN mitogenomes, and 11 of 14 SNPs (78.57%) between the WBPHHN and WBPHYN mitogenomes were found in PCGs. Eight of 13 PCGs, including ND2, COX1, COX3, ND3, ND5, ND4, CytB, and ND1, contained one or more SNPs. Four of eight PCGs, COX3, ND5, ND4, and CytB, contained one non-synonymous SNP in each pair of WBPH mitogenomes. These non-synonymous SNPs can affect the function of the PCGs as reported for L. striatellus [93]. These PCGs can be a potential target to develop molecular markers to distinguish populations of WBPHs once more mitogenomes of WBPHs isolated from different locations are available.
The numbers of SNPs and INDEL regions identified from the three WBPH mitogenomes were relatively smaller than those of L. striatellus [63,79], N. lugens [76], and Chilo supressalis (Walker) [62], of which samples were captured in Korea and China, indicating that the genetic diversity of WBPH might be lower than those of the three species. Furthermore, the numbers of intraspecific variations in WBPHs were also smaller than those of Aphis gossypii Glover [61,94,95] and Spodoptera frugiperda (J. E. Smith) [64] but were larger in number than those of Korean samples of Hipparchia autonoe (Esper) [96] and Alphitobius diaperinus Panzer [58].

3.4. Identification and Comparison of Simple Sequence Repeats on WBPH Mitogenomes

Simple sequence repeats (SSRs), which can be utilized as molecular markers to distinguish insect species [97,98] and to identify cryptic insect species [99], were identified from the three WBPH mitogenomes. The WBPHTA and WBPHHN mitogenomes displayed 25 normal SSRs, 69 potential SSRs, and 9 extended SSRs, whereas the WBPHHN mitogenome exhibited 24 normal SSRs (Table 2), 70 potential SSRs, and 9 extended SSRs (Figure 6A; Supplementary Table S2). The differences in the number of monoSSRs and pentaSSRs among the three mitogenomes were one (Figure 6A). This intraspecific difference in SSRs is similar to that of Stegobium paniceum (Linnaeus, 1758) (one difference in monoSSR, diSSR, and hexaSSR; Park et al., under review) and Monomorium pharaonis (Linnaeus, 1758) (one difference in pentaSSR and decaSSR; Park et al., under revision).
Comparisons of flanking sequences of each SSR identified from the three WBPH mitogenomes using the SSRDB (see Materials and Methods), identified 108 SSR groups: 98 out of 108 SSR groups (90.74%) contained three SSRs originating from three WBPH mitogenomes, called common SSRs (Figure 6B). Three of the five SSR groups (60.00%), covering two SSRs from the two mitogenomes, contained SSRs of WBPHHN and WBPHYN, captured in China, while two of the five SSR groups (40.00%) were from WBPHHN and WBPHTA (Table 3; Figure 6B). Two of the five SSR groups consisting of the two Chinese WBPHs were located in the CTYB gene (SSRGroup 75 and SSRGroup 103; Table 3), whereas SSRGroup 34 contains the monoSSRs originating from WBPHHN and WBPHTA (Table 3). Furthermore, singleton SSR groups consisted of two SSRs from WBPHHN and three SSRs from WBPHTA (Table 3; Figure 6B). All five singleton SSRs were in the intergenic regions: (i) the region between ND6 and tRNA-Pro and (ii) the putative control region (Table 3). Interestingly, WBPHYN did not have any singleton SSR (Figure 6B), indicating that the WBPHYN mitogenome does not have any unique SNPs or INDELs in SSRs. The ratio of singleton SSRs of WBPH mitogenomes was similar to that of M. pharaonis (7.00%; Park et al., under revision) but was lower than that of S. paniceum (12.85%; Park et al., under review).
The SSRs identified from the three WBPH mitogenomes were densely distributed in the putative control regions as well as in the ND4 and ND1 genic regions. Interestingly, the 5′ part of the putative control region displayed a high density of SSRs in a conserved manner across the three mitogenomes, while the 3′ part of the putative control regions exhibited a low density of SSRs with variable manners across the three mitogenomes). This correlation between SSR density and intraspecific variations will be investigated more in other insect species, which can be used as a guide for developing efficient molecular markers using SSRs. The intraspecific SSRs identified in this study could be potential candidates for developing markers with WBPH mitogenomes which will be sequenced in near future to distinguish geographical populations and to understand the migration pathway of WBPH.

3.5. Phylogenetic Tree of 32 Delphacidae Mitogenomes including Three WBPH Mitogenomes

Maximum-likelihood (ML) and Bayesian inference (BI) phylogenetic trees of 32 mitogenomes of Delphacidae including three WBPH mitogenomes and one outgroup species, Haplaxius crudus van Duzee, 1907, were constructed. Among the 32 Delphacidae mitogenomes, only one mitogenome, Stenocranus matsumurai Metcalf, 1943(GenBank accession number: MH293469), belongs to the subfamily Stenocraninae, while the remaining 31 mitogenomes belong to the subfamily Delphacinae. Phylogenetic trees demonstrated that both subfamilies were clearly distinct from each other (Figure 7). In addition, all branches except one (see grey arrow in Figure 6) were supported by the high supportive values of both trees (Figure 1), displaying a rigid phylogenetic relationship within the family Delphacidae. This is congruent with the previous phylogenetic studies [46,100,101], supporting that the phylogenetic relationship of the 30 Delphacidae species become more supportive in comparison to the incongruent cases of molecular phylogeny based on between marker sequences and complete mitogenomes [102,103,104]. The exceptional clade displaying low supportive values of ML (52; Figure 7) was also presented lower supportive values of both ML and BI trees (Clade III) in the previous phylogenetic study [46]. However, the bootstrap value of BI was increased to 0.9995 (Figure 7), indicating that complete mitogenome contributed increment of supportive values in the phylogenetic tree. If more complete mitogenomes of neighbor genera of Sogata, such as Miranus, Hadeodelphax, Liburniella, and Neometopina, are available in the future, the phylogenetic relationship of this clade is expected to become clearer.
The BI tree demonstrated that three WBPH mitogenomes were clustered in one clade; while the ML tree demonstrated that WBPHTA and WBPHHN were clustered together, suggesting the possibility that the WBPHTA sample may be from a similar region to the Hainan province in China, where the WBPHHN isolate was captured [8], together with the fact that WBPH cannot overwinter in the Korean peninsula [1]. Moreover, the population structure of WBPHs isolated in Yunnan and Shandong provinces in China and five Southeast Asian countries including the Greater Mekong subregion (GMS) are considered to be important overwintering sites, displayed one group regardless of geographical distributions by principal coordinates analysis with a 635-bpmitochondrial COI sequence data [14]. Further studies with more mitogenomes of WBPHs are required to determine the origin of Korean WBPHs as well as the immigration routes of WBPH in the Northeast Asian area. Complete mitogenomes of geographically dispersed WBPH populations will be one of the potential data for further population genetic studies to understand the WBPH migration pathway in Asian countries.

4. Conclusions

In this study, we reported a new complete mitogenome of WBPH collected in Korea (named as WBPHTA) and firstly identified heteroplasmy in WBPH and Delphacidae. The heteroplasmy resulted in the amino acid substitution in COX3, causing not severe conformational change based on the prediction of three-dimensional structure. In addition, this heteroplasmy was not found in the two wild populations in Korea, suggesting that continuous selection pressure may cause this heteroplasmy. Intraspecific variations and simple sequence repeats (SSRs) were identified among the three WBPH mitogenomes, suggesting that these can be a potential target to develop molecular markers to distinguish populations of WBPHs from different locations. Phylogenetic analysis suggested that Delphacinae is monophyletic and WBPH, as one group, is clearly divided with closely related Sogatella species. The heteroplasmy, the firstly reported in WBPH mitogenome, suggests an additional step to check the polymorphic sites during the assembly. In addition, intraspecific variations in WBPH mitogenomes can be useful to understand its genetic diversity as well as to develop useful markers and to understand the migration of geographically dispersed WBPH populations.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/insects12121066/s1, Table S1: Summary on a new mitochondrial genome of Sogatella furcifera collected in Korea, Table S2: List of potential and extended SSRs identified in the WBPHTA mitogenome.

Author Contributions

Conceptualization, J.P. (Jongsun Park) and B.Y.S.; methodology, J.P. (Jongsun Park); software, H.X. and J.P. (Jonghyun Park); validation, J.P. (Jongsun Park) and B.Y.S.; formal analysis, J.P. (Jongsun Park), H.X. and J.P. (Jonghyun Park); investigation, J.P. (Jongsun Park); data curation, J.P. (Jongsun Park), H.X. and J.P. (Jonghyun Park); writing—original draft preparation, J.P. (Jongsun Park) and B.Y.S.; writing—review and editing, J.P. (Jongsun Park) and B.Y.S.; visualization, J.P. (Jongsun Park) and H.X.; supervision, J.P. (Jongsun Park); project administration, J.P. (Jongsun Park) and B.Y.S.; funding acquisition, J.P. (Jongsun Park) All authors have read and agreed to the published version of the manuscript.

Funding

This study was carried out with the support of the “InfoBoss Research Grant (No. IBG-0041)” funded by J.P. (Jongsun Park).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Mitochondrial genome sequence used in this study can be accessed via accession number MK907866 in NCBI GenBank.

Acknowledgments

The authors would like to thank the anonymous reviewers and the editor for the improved quality of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kisimoto, R.; Sogawa, K. Migration of the brown planthopper Nilaparvata lugens and the white-backed planthopper Sogatella furciferain East Asia: The role of weather and climate. In Insect Migration: Tracking Resources through Space and Time; Drake, V.A., Gatehouse, A.G., Eds.; Cambridge University Press: Cambridge, UK, 1995; pp. 67–92. [Google Scholar]
  2. Yan, X.H.; Liu, H.; Zhao, Z.M.; Xiao, X.H.; Cheng, D.F. Occurrence of the brown planthopper Nilaparvata lugens and the white-backed planthopper Sogatella furcifera in Xiushan of Chongqing. Plant Prot. 2012, 38, 128–132. [Google Scholar]
  3. Park, J.; An, J.-H.; Kim, Y.; Kim, D.; Yang, B.-G.; Kim, T. Database of National Species List of Korea: The taxonomical systematics platform for managing scientific names of Korean native species. J. Species Res. 2020, 9, 233–246. [Google Scholar]
  4. Zhu, Z.-R.; Cheng, J. Sucking rates of the white-backed planthopper Sogatella furcifera (Horv.) (Homoptera, Delphacidae) and yield loss of rice. J. Pest Sci. 2002, 75, 113–117. [Google Scholar] [CrossRef]
  5. Khan, Z.; Saxena, R. Behavioral and physiological responses of Sogatella furcifera (Homoptera: Delphacidae) to selected resistant and susceptible rice cultivars. J. Econ. Entomol. 1985, 78, 1280–1286. [Google Scholar] [CrossRef]
  6. Khatri, A.; Gangrade, G.; Rathore, V. Studies on the crop losses in rice caused by the white-backed planthopper (Sogatella furcifera) and the economic injury level in India. Int. J. Pest Manag. 1983, 29, 220–223. [Google Scholar] [CrossRef]
  7. Wang, L.; Tang, N.; Gao, X.; Chang, Z.; Zhang, L.; Zhou, G.; Guo, D.; Zeng, Z.; Li, W.; Akinyemi, I.A. Genome sequence of a rice pest, the white-backed planthopper (Sogatella furcifera). GigaScience 2017, 6, giw004. [Google Scholar]
  8. Zhang, K.-J.; Zhu, W.-C.; Rong, X.; Liu, J.; Ding, X.-L.; Hong, X.-Y. The complete mitochondrial genome sequence of Sogatella furcifera (Horváth) and a comparative mitogenomic analysis of three predominant rice planthoppers. Gene 2014, 533, 100–109. [Google Scholar] [CrossRef]
  9. Cheng, J.A. Rice planthopper problems and relevant causes in China. In Planthoppers: New Threats to the Sustainability of Intensive Rice Production Systems in Asia; Heong, K., Hardy, B., Eds.; International Rice Research Institute: Los Baños, Philippines, 2009; pp. 157–178. [Google Scholar]
  10. Cho, Y.-S.; Lee, D.-K.; Choe, Z.-R.; Han, M.-S.; Pellerin, K. Conservation of biodiversity and its ecological importance of Korean paddy field. J. Crop Sci. 2006, 51, 497–504. [Google Scholar]
  11. Bottrell, D.G.; Schoenly, K.G. Resurrecting the ghost of green revolutions past: The brown planthopper as a recurring threat to high-yielding rice production in tropical Asia. J. Asia-Pac. Entomol. 2012, 15, 122–140. [Google Scholar] [CrossRef]
  12. Han, L.; Zhang, J.-T.; Wang, M.-M.; Zhu, K.-X.; Wang, X.-Y. Mitochondrial DNA diversity and population structure of Laodelphax striatellus across a broad geographic area in China. Mitochondrial DNA Part A 2020, 31, 346–354. [Google Scholar] [CrossRef]
  13. Kwon, D.H.; Jeong, I.-H.; Lee, S.W.; Lee, S.H. Comparing the genetic diversity and structure of indigenous Korean and Chinese populations of Laodelphax striatellus Fallén using mitochondrial haplotypes. J. Asia-Pac. Entomol. 2018, 21, 233–238. [Google Scholar] [CrossRef]
  14. Yang, N.; Dong, Z.; Chen, A.; Yin, Y.; Li, X.; Chu, D. Migration of Sogatella furcifera between the Greater Mekong Subregion and northern China revealed by mtDNA and SNP. BMC Evol. Biol. 2020, 20, 1–10. [Google Scholar] [CrossRef] [PubMed]
  15. Matsumoto, Y.; Matsumura, M.; Sanada-Morimura, S.; Hirai, Y.; Sato, Y.; Noda, H. Mitochondrial cox sequences of Nilaparvata lugens and Sogatella furcifera (Hemiptera, Delphacidae): Low specificity among Asian planthopper populations. Bull. Entomol. Res. 2013, 103, 382. [Google Scholar] [CrossRef] [PubMed]
  16. Li, X.-y.; Chu, D.; Yin, Y.-q.; Zhao, X.-q.; Chen, A.-d.; Khay, S.; Douangboupha, B.; Kyaw, M.M.; Kongchuensin, M.; Ngo, V.V. Possible source populations of the white-backed planthopper in the Greater Mekong Subregion revealed by mitochondrial DNA analysis. Sci. Rep. 2016, 6, 39167. [Google Scholar] [CrossRef] [Green Version]
  17. Park, J.; Jung, J.K.; Lee, G.-S.; Cho, J.; Koh, Y.H.; Seo, B.Y. Comparative analyses of Laodelphax striatellus mitochondrial genomes: Insight haplotypes of mitogenomes in three East Asian countries. In Proceedings of the 2019 Fall International Conference of KSAE, Pyoungchang, Korea, 24 October 2019; p. 110. [Google Scholar]
  18. Metzker, M.L. Sequencing technologies—The next generation. Nat. Rev. Genet. 2010, 11, 31–46. [Google Scholar] [CrossRef] [Green Version]
  19. Goodwin, S.; McPherson, J.D.; McCombie, W.R. Coming of age: Ten years of next-generation sequencing technologies. Nat. Rev. Genet. 2016, 17, 333–351. [Google Scholar] [CrossRef]
  20. Bleidorn, C. Third generation sequencing: Technology and its potential impact on evolutionary biodiversity research. Syst. Biodivers. 2016, 14, 1–8. [Google Scholar] [CrossRef]
  21. Zerbino, D.R.; Birney, E. Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008, 18, 821–829. [Google Scholar] [CrossRef] [Green Version]
  22. Peng, Y.; Leung, H.C.; Yiu, S.-M.; Chin, F.Y. T-IDBA: A de novo iterative de Bruijn graph assembler for transcriptome. In Proceedings of the International Conference on Research in Computational Molecular Biology, Vancouver, BC, Canada, 28–31 March 2011; pp. 337–338. [Google Scholar]
  23. Peng, Y.; Leung, H.C.; Yiu, S.-M.; Lv, M.-J.; Zhu, X.-G.; Chin, F.Y. IDBA-tran: A more robust de novode Bruijn graph assembler for transcriptomes with uneven expression levels. Bioinformatics 2013, 29, i326–i334. [Google Scholar] [CrossRef] [Green Version]
  24. Xie, Y.; Wu, G.; Tang, J.; Luo, R.; Patterson, J.; Liu, S.; Huang, W.; He, G.; Gu, S.; Li, S. SOAPdenovo-Trans: De novo transcriptome assembly with short RNA-Seq reads. Bioinformatics 2014, 30, 1660–1666. [Google Scholar] [CrossRef] [Green Version]
  25. Luo, R.; Liu, B.; Xie, Y.; Li, Z.; Huang, W.; Yuan, J.; He, G.; Chen, Y.; Pan, Q.; Liu, Y. SOAPdenovo2: An empirically improved memory-efficient short-read de novo assembler. GigaScience 2012, 1, 18. [Google Scholar] [CrossRef]
  26. Park, J.; Xi, H. Genome Archive (R): Standardized genome repository for supporting large-scale genome analyses. In Proceedings of the Plant and Animal Genome XXVI Conference, San Diego, CA, USA, 13–17 January 2018. [Google Scholar]
  27. Lee, W.; Park, J.; Choi, J.; Jung, K.; Park, B.; Kim, D.; Lee, J.; Ahn, K.; Song, W.; Kang, S. IMGD: An integrated platform supporting comparative genomics and phylogenetics of insect mitochondrial genomes. BMC Genom. 2009, 10, 1–16. [Google Scholar] [CrossRef] [Green Version]
  28. Quail, M.A.; Kozarewa, I.; Smith, F.; Scally, A.; Stephens, P.J.; Durbin, R.; Swerdlow, H.; Turner, D.J. A large genome center’s improvements to the Illumina sequencing system. Nat. Methods 2008, 5, 1005–1010. [Google Scholar] [CrossRef] [Green Version]
  29. Bentley, D.R.; Balasubramanian, S.; Swerdlow, H.P.; Smith, G.P.; Milton, J.; Brown, C.G.; Hall, K.P.; Evers, D.J.; Barnes, C.L.; Bignell, H.R. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 2008, 456, 53–59. [Google Scholar] [CrossRef]
  30. Cuomo, C.A.; Güldener, U.; Xu, J.-R.; Trail, F.; Turgeon, B.G.; Di Pietro, A.; Walton, J.D.; Ma, L.-J.; Baker, S.E.; Rep, M. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 2007, 317, 1400–1402. [Google Scholar] [CrossRef] [Green Version]
  31. Jaillon, O.; Aury, J.-M.; Noel, B.; Policriti, A.; Clepet, C.; Casagrande, A.; Choisne, N.; Aubourg, S.; Vitulo, N.; Jubin, C. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007, 449, 463–467. [Google Scholar]
  32. Kocher, A.; Kamilari, M.; Lhuillier, E.; Coissac, E.; Péneau, J.; Chave, J.; Murienne, J. Shotgun assembly of the assassin bug Brontostoma colossus mitochondrial genome (Heteroptera, Reduviidae). Gene 2014, 552, 184–194. [Google Scholar] [CrossRef]
  33. Yang, S.; Li, X.; Cai, L.-G.; Qian, Z.-Q. Characterization of the complete mitochondrial genome of Formica selysi (Insecta: Hymenoptera: Formicidae: Formicinae). Mitochondrial DNA Part A 2016, 27, 3378–3380. [Google Scholar] [CrossRef]
  34. Linard, B.; Arribas, P.; Andujar, C.; Crampton-Platt, A.; Vogler, A. The mitogenome of Hydropsyche pellucidula (Hydropsychidae): First gene arrangement in the insect order Trichoptera. Mitochondrial DNA Part A 2017, 28, 71–72. [Google Scholar] [CrossRef] [Green Version]
  35. Zhang, Q.-X.; Guan, D.-L.; Niu, Y.; Sang, L.-Q.; Zhang, X.-X.; Xu, S.-Q. Characterization of the complete mitochondrial genome of the Asian planthopper Ricania speculum (Hemiptera: Fulgoroidea: Ricannidae). Conserv. Genet. Resour. 2016, 8, 463–466. [Google Scholar] [CrossRef]
  36. Park, J.; Xi, H.; Park, J. Complete mitochondrial genome of the acrobat ant Crematogaster teranishii Santschi, 1930 (Formicidae; Hymenoptera). Mitochondrial DNA Part B 2021, 6, 593–595. [Google Scholar] [CrossRef]
  37. Lee, H.; Park, J.; Xi, H.; Lee, G.-S.; Kim, I.; Park, J.; Lee, W. The complete mitochondrial genome of Ricania speculum (Walker, 1851) (Hemiptera: Ricaniidae): Investigation of intraspecific variations on mitochondrial genome. Mitochondrial DNA Part B 2020, 5, 3796–3798. [Google Scholar] [CrossRef]
  38. Liu, J.-H.; Jia, P.-F.; Fu, J.-Q.; Dan, W.-L.; Yang, L.-Y.; Wang, Q.-M.; Li, Z.-N. Characterization of mitochondrial genome and phylogenetic implications for Chinese black ant, Polyrhachis dives (Hymenoptera: Formicidae). Mitochondrial DNA Part B 2017, 2, 679–680. [Google Scholar] [CrossRef]
  39. Birky Jr, C.W. Transmission genetics of mitochondria and chloroplasts. Annu. Rev. Genet. 1978, 12, 471–512. [Google Scholar] [CrossRef]
  40. Avise, J.C. Phylogeography: The History and Formation of Species; Harvard University Press: Cambridge, MA, USA, 2000; pp. 1–464. [Google Scholar]
  41. Solignac, M.; Monnerot, M.; Mounolou, J.-C. Mitochondrial DNA heteroplasmy in Drosophila mauritiana. Proc. Natl. Acad. Sci. USA 1983, 80, 6942–6946. [Google Scholar] [CrossRef] [Green Version]
  42. Solignac, M.; Génermont, J.; Monnerot, M.; Mounolou, J.-C. Genetics of mitochondria in Drosophila: mtDNA inheritance in heteroplasmic strains of D. mauritiana. Mol. Gen. Genet. 1984, 197, 183–188. [Google Scholar] [CrossRef]
  43. Boyce, T.M.; Zwick, M.E.; Aquadro, C.F. Mitochondrial DNA in the bark weevils: Size, structure and heteroplasmy. Genetics 1989, 123, 825–836. [Google Scholar] [CrossRef]
  44. Brown, J.R.; Beckenbach, K.; Beckenbach, A.T.; Smith, M.J. Length variation, heteroplasmy and sequence divergence in the mitochondrial DNA of four species of sturgeon (Acipenser). Genetics 1996, 142, 525–535. [Google Scholar] [CrossRef]
  45. Paduan, K.D.S.; Ribolla, P.E.M. Mitochondrial DNA polymorphism and heteroplasmy in populations of Aedes aegypti in Brazil. J. Med. Entomol. 2008, 45, 59–67. [Google Scholar] [CrossRef]
  46. Huang, Y.-X.; Zheng, L.-F.; Bartlett, C.R.; Qin, D.-Z. Resolving phylogenetic relationships of Delphacini and Tropidocephalini (Hemiptera: Delphacidae: Delphacinae) as inferred from four genetic loci. Sci. Rep. 2017, 7, 3319. [Google Scholar] [CrossRef]
  47. Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef] [Green Version]
  48. Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv 2013, arXiv:1303.3997. [Google Scholar]
  49. Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; Durbin, R. The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25, 2078–2079. [Google Scholar] [CrossRef] [Green Version]
  50. Park, J.; Xi, H.; Kim, Y.; Kim, M. Complete genome sequence of Lentilactobacillus parabuchneri strain KEM. Microbiol. Resour. Announc. 2021, 10, e01208-20. [Google Scholar] [CrossRef]
  51. Kim, M.; Xi, H.; Park, S.; Yun, Y.; Park, J. Genome-wide comparative analyses of GATA transcription factors among seven Populus genomes. Sci. Rep. 2021, 11, 16578. [Google Scholar] [CrossRef]
  52. Seo, B.Y.; Cho, J.; Lee, G.-S.; Park, J.; Park, J. The complete mitochondrial genome of Exorista japonica (Townsend, 1909) (Diptera: Tachinidae). Mitochondrial DNA Part B 2019, 4, 2244–2245. [Google Scholar] [CrossRef]
  53. Park, J.; Xi, H.; Park, J. The complete mitochondrial genome of Rotunda rotundapex (Miyata & Kishida, 1990) (Lepidoptera: Bombycidae). Mitochondrial DNA Part B 2020, 5, 355–357. [Google Scholar]
  54. Laslett, D.; Canbäck, B. ARWEN: A program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 2007, 24, 172–175. [Google Scholar] [CrossRef] [Green Version]
  55. Waterhouse, A.; Bertoni, M.; Bienert, S.; Studer, G.; Tauriello, G.; Gumienny, R.; Heer, F.T.; de Beer, T.A.P.; Rempfer, C.; Bordoli, L. SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Res. 2018, 46, W296–W303. [Google Scholar] [CrossRef] [Green Version]
  56. Katoh, K.; Standley, D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef] [Green Version]
  57. Choi, N.J.; Lee, B.-C.; Park, J.; Park, J. The complete mitochondrial genome of Nilaparvata lugens (Stål, 1854) captured in China (Hemiptera: Delphacidae): Investigation of intraspecies variations between countries. Mitochondrial DNA Part B 2019, 4, 1677–1678. [Google Scholar] [CrossRef]
  58. Wang, Q.; Mao, L.-H.; Ding, B.; Li, M.-T.; Fu, Z.-X.; Deng, H.-P. The complete chloroplast genome of Plantago fengdouensis (Plantaginaceae): An endemic and endangered species from China. Mitochondrial DNA Part B 2020, 5, 51–52. [Google Scholar] [CrossRef] [Green Version]
  59. Jung, Y.J.; Jo, J.; Bae, Y.; Xi, H.; Seol, M.-A.; Yoo, S.-H.; Park, J.; Park, C. The complete mitochondrial genome of Myzus persicae (Sulzer, 1776; Hemiptera: Aphididae) isolated in Korea. Mitochondrial DNA Part B 2021, 6, 10–12. [Google Scholar] [CrossRef]
  60. Choi, N.J.; Lee, B.-C.; Park, J.; Park, J. The complete mitochondrial genome of Nilaparvata lugens (Stål, 1854) captured in Guangxi Province, China (Hemiptera: Delphacidae): Identification of the origin of N. lugens migrated to Korea. Mitochondrial DNA Part B 2020, 5, 1960–1961. [Google Scholar] [CrossRef]
  61. Park, J.; Lee, J.; Lee, W. The complete mitochondrial genome of Aphis gossypii Glover, 1877 (Hemiptera: Aphididae) isolated from Leonurus japonicus in Korea. Mitochondrial DNA Part B 2021, 6, 62–65. [Google Scholar] [CrossRef]
  62. Park, J.; Xi, H.; Kwon, W.; Park, C.-G.; Lee, W. The complete mitochondrial genome sequence of Korean Chilo suppressalis (Walker, 1863) (Lepidoptera: Crambidae). Mitochondrial DNA Part B 2019, 4, 850–851. [Google Scholar] [CrossRef] [Green Version]
  63. Seo, B.Y.; Jung, J.K.; Ho Koh, Y.; Park, J. The complete mitochondrial genome of Laodelphax striatellus (Fallén, 1826) (Hemiptera: Delphacidae) collected in a southern part of Korean Peninsula. Mitochondrial DNA Part B 2019, 4, 2242–2243. [Google Scholar] [CrossRef]
  64. Seo, B.Y.; Lee, G.-S.; Park, J.; Xi, H.; Lee, H.; Lee, J.; Park, J.; Lee, W. The complete mitochondrial genome of the fall armyworm, Spodoptera frugiperda Smith, 1797 (Lepidoptera; Noctuidae), firstly collected in Korea. Mitochondrial DNA Part B 2019, 4, 3918–3920. [Google Scholar] [CrossRef] [Green Version]
  65. Lee, J.; Park, J.; Xi, H.; Park, J. Comprehensive analyses of the complete mitochondrial genome of Figulus binodulus (Coleoptera: Lucanidae). J. Insect Sci. 2020, 20, 10. [Google Scholar] [CrossRef]
  66. Kim, Y.; Park, J.; Chung, Y. Comparative analysis of chloroplast genome of Dysphania ambrosioides (L.) Mosyakin & Clemants understanding phylogenetic relationship in genus Dysphania R. Br. Korean J. Plant Resour. 2019, 32, 644–668. [Google Scholar]
  67. Park, J.; Xi, H.; Kim, Y.; Nam, S.; Heo, K.-I. The complete mitochondrial genome of new species candidate of Rosa rugosa (Rosaceae). Mitochondrial DNA Part B 2020, 5, 3453–3455. [Google Scholar] [CrossRef]
  68. Park, J.; Xi, H.; Kim, Y. The complete chloroplast genome of Arabidopsis thaliana isolated in Korea (Brassicaceae): An investigation of intraspecific variations of the chloroplast genome of Korean A. thaliana. Int. J. Genom. 2020, 2020, 3236461. [Google Scholar] [CrossRef]
  69. Park, J.; Min, J.; Kim, Y.; Chung, Y. The Comparative analyses of six complete chloroplast genomes of morphologically diverse Chenopodium albumL. (Amaranthaceae) collected in Korea. Int. J. Genom. 2021, 2021, 6643444. [Google Scholar]
  70. Choi, N.J.; Xi, H.; Park, J. A Comparative analyses of the complete mitochondrial genomes of fungal endosymbionts in Sogatella furcifera, white-backed planthoppers. Int. J. Genom. 2021, 2021, 6652508. [Google Scholar] [CrossRef]
  71. Nguyen, L.-T.; Schmidt, H.A.; Von Haeseler, A.; Minh, B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 2015, 32, 268–274. [Google Scholar] [CrossRef]
  72. Ronquist, F.; Teslenko, M.; Van Der Mark, P.; Ayres, D.L.; Darling, A.; Höhna, S.; Larget, B.; Liu, L.; Suchard, M.A.; Huelsenbeck, J.P. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012, 61, 539–542. [Google Scholar] [CrossRef] [Green Version]
  73. Cameron, S.L. Insect mitochondrial genomics: Implications for evolution and phylogeny. Annu. Rev. Entomol. 2014, 59, 95–117. [Google Scholar] [CrossRef] [Green Version]
  74. Boore, J.L. Animal mitochondrial genomes. Nucleic Acids Res. 1999, 27, 1767–1780. [Google Scholar] [CrossRef] [Green Version]
  75. Zhang, D.-X.; Hewitt, G.M. Insect mitochondrial control region: A review of its structure, evolution and usefulness in evolutionary studies. Biochem. Syst. Ecol. 1997, 25, 99–120. [Google Scholar] [CrossRef]
  76. Park, J.; Kwon, W.; Park, J.; Kim, H.-J.; Lee, B.-C.; Kim, Y.; Choi, N.J. The complete mitochondrial genome of Nilaparvata lugens (Stål, 1854) captured in Korea (Hemiptera: Delphacidae). Mitochondrial DNA Part B 2019, 4, 1674–1676. [Google Scholar] [CrossRef] [Green Version]
  77. Zhang, K.-J.; Zhu, W.-C.; Rong, X.; Zhang, Y.-K.; Ding, X.-L.; Liu, J.; Chen, D.-S.; Du, Y.; Hong, X.-Y. The complete mitochondrial genomes of two rice planthoppers, Nilaparvata lugens and Laodelphax striatellus: Conserved genome rearrangement in Delphacidae and discovery of new characteristics of atp8 and tRNA genes. BMC Genom. 2013, 14, 417. [Google Scholar] [CrossRef] [Green Version]
  78. Lv, L.; Peng, X.; Jing, S.; Liu, B.; Zhu, L.; He, G. Intraspecific and interspecific variations in the mitochondrial genomes of Nilaparvata (Hemiptera: Delphacidae). J. Econ. Entomol. 2015, 108, 2021–2029. [Google Scholar] [CrossRef]
  79. Park, J.; Jung, J.K.; Ho Koh, Y.; Park, J.; Seo, B.Y. The complete mitochondrial genome of Laodelphax striatellus (Fallén, 1826) (Hemiptera: Delphacidae) collected in a mid-western part of Korean peninsula. Mitochondrial DNA Part B 2019, 4, 2229–2230. [Google Scholar] [CrossRef]
  80. Robison, G.; Balvin, O.; Schal, C.; Vargo, E.; Booth, W. Extensive mitochondrial heteroplasmy in natural populations of a resurging human pest, the bed bug (Hemiptera: Cimicidae). J. Med. Entomol. 2015, 52, 734–738. [Google Scholar] [CrossRef] [Green Version]
  81. Meusel, M.S.; Moritz, R.F. Transfer of paternal mitochondrial DNA during fertilization of honeybee (Apis mellifera L.) eggs. Curr. Genet. 1993, 24, 539–543. [Google Scholar] [CrossRef]
  82. Meza-Lázaro, R.N.; Poteaux, C.; Bayona-Vásquez, N.J.; Branstetter, M.G.; Zaldívar-Riverón, A. Extensive mitochondrial heteroplasmy in the neotropical ants of the Ectatomma ruidum complex (Formicidae: Ectatomminae). Mitochondrial DNA Part A 2018, 29, 1203–1214. [Google Scholar] [CrossRef]
  83. Kang, A.R.; Kim, M.J.; Park, I.A.; Kim, K.Y.; Kim, I. Extent and divergence of heteroplasmy of the DNA barcoding region in Anapodisma miramae (Orthoptera: Acrididae). Mitochondrial DNA Part A 2016, 27, 3405–3414. [Google Scholar] [CrossRef]
  84. Nardi, F.; Carapelli, A.; Fanciulli, P.P.; Dallai, R.; Frati, F. The complete mitochondrial DNA sequence of the basal hexapod Tetrodontophora bielanensis: Evidence for heteroplasmy and tRNA translocations. Mol. Biol. Evol. 2001, 18, 1293–1304. [Google Scholar] [CrossRef] [Green Version]
  85. Nunes, M.D.; Dolezal, M.; Schlötterer, C. Extensive paternal mt DNA leakage in natural populations of Drosophila melanogaster. Mol. Ecol. 2013, 22, 2106–2117. [Google Scholar] [CrossRef] [Green Version]
  86. Baião, G.C.; Strunov, A.; Heyworth, E.; Schneider, D.I.; Thoma, J.; Klasson, L.; Miller, W.J. Persistence and invasiveness of high-level heteroplasmy through biparental transmission of a selfish mitochondrion in Drosophila. bioRxiv 2020. [Google Scholar] [CrossRef]
  87. Van Leeuwen, T.; Vanholme, B.; Van Pottelberge, S.; Van Nieuwenhuyse, P.; Nauen, R.; Tirry, L.; Denholm, I. Mitochondrial heteroplasmy and the evolution of insecticide resistance: Non-Mendelian inheritance in action. Proc. Natl. Acad. Sci. USA 2008, 105, 5980–5985. [Google Scholar] [CrossRef] [Green Version]
  88. Vielba-Fernández, A.; Bellón-Gómez, D.; Torés, J.A.; de Vicente, A.; Pérez-García, A.; Fernández-Ortuño, D. Heteroplasmy for the cytochrome b gene in Podosphaera xanthii and its role in resistance to QoI fungicides in Spain. Plant Dis. 2018, 102, 1599–1605. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  89. Villani, S.M.; Cox, K.D. Heteroplasmy of the cytochrome b gene in Venturia inaequalis and its involvement in quantitative and practical resistance to trifloxystrobin. Phytopathology 2014, 104, 945–953. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  90. Lesemann, S.; Schimpke, S.; Dunemann, F.; Deising, H. Mitochondrial heteroplasmy for the cytochrome b gene controls the level of strobilurin resistance in the apple powdery mildew fungus Podosphaera leucotricha (Ell. & Ev.) ES Salmon. J. Plant Dis. Prot. 2006, 113, 259–266. [Google Scholar]
  91. Pridgeon, J.W.; Becnel, J.J.; Clark, G.G.; Linthicum, K.J. Permethrin induces overexpression of cytochrome c oxidase subunit 3 in Aedes aegypti. J. Med. Entomol. 2009, 46, 810–819. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  92. Fenn, J.; Cameron, S.; Whiting, M. The complete mitochondrial genome sequence of the Mormon cricket (Anabrus simplex: Tettigoniidae: Orthoptera) and an analysis of control region variability. Insect Mol. Biol. 2007, 16, 239–252. [Google Scholar] [CrossRef] [PubMed]
  93. Kim, Y.; Heo, K.-I.; Park, J. The second complete chloroplast genome sequence of Pseudostellaria palibiniana (Takeda) Ohwi (Caryophyllaceae): Intraspecies variations based on geographical distribution. Mitochondrial DNA Part B 2019, 4, 1310–1311. [Google Scholar] [CrossRef] [Green Version]
  94. Bae, Y.; Park, J.; Lee, W. The complete mitochondrial genome of Aphis gossypii Glover, 1877 (Hemiptera: Aphididae) isolated from Plantago asiatica in Korea. Mitochondrial DNA Part B 2020, 5, 2896–2898. [Google Scholar] [CrossRef]
  95. Park, J.; Xi, H.; Kim, Y.; Park, J.; Lee, W. The complete mitochondrial genome of Aphis gossypii Glover, 1877 (Hemiptera: Aphididae) collected in Korean Peninsula. Mitochondrial DNA Part B 2019, 4, 3007–3009. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  96. Lee, Y.-D.; Lee, J.; Kim, D.-S.; Park, J.; Xi, H.; Roh, J.; Kim, D.-S.; Nam, S.J.; Kim, S.-K.; Song, J.-Y. The complete mitochondrial genome of Hipparchia autonoe (Esper, 1783) (Lepidoptera: Nymphalidae): Investigation of intraspecific variations on mitochondrial genome. Mitochondrial DNA Part B 2020, 5, 1542–1544. [Google Scholar] [CrossRef]
  97. Simon, C.; Frati, F.; Beckenbach, A.; Crespi, B.; Liu, H.; Flook, P. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann. Entomol. Soc. Am. 1994, 87, 651–701. [Google Scholar] [CrossRef]
  98. Mousson, L.; Dauga, C.; Garrigues, T.; Schaffner, F.; Vazeille, M.; Failloux, A.-B. Phylogeography of Aedes (Stegomyia) aegypti (L.) and Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae) based on mitochondrial DNA variations. Genet. Res. 2005, 86, 1–11. [Google Scholar] [CrossRef]
  99. Burger, T.D.; Shao, R.; Barker, S.C. Phylogenetic analysis of mitochondrial genome sequences indicates that the cattle tick, Rhipicephalus (Boophilus) microplus, contains a cryptic species. Mol. Phylogenet. Evol. 2014, 76, 241–253. [Google Scholar] [CrossRef] [PubMed]
  100. Huang, Y.-X.; Ren, F.-J.; Bartlett, C.R.; Wei, Y.-S.; Qin, D.-Z. Contribution to the mitogenome diversity in Delphacinae: Phylogenetic and ecological implications. Genomics 2020, 112, 1363–1370. [Google Scholar] [CrossRef]
  101. Song, N.; Liang, A.-P. A preliminary molecular phylogeny of planthoppers (Hemiptera: Fulgoroidea) based on nuclear and mitochondrial DNA sequences. PLoS ONE 2013, 8, e58400. [Google Scholar] [CrossRef] [Green Version]
  102. Park, J.; Park, C.-H.; Park, J. Complete mitochondrial genome of the H3 haplotype Argentine ant Linepithema humile (Mayr, 1868) (Formicidae; Hymenoptera). Mitochondrial DNA Part B 2021, 6, 786–788. [Google Scholar] [CrossRef] [PubMed]
  103. Chen, Z.; Zhou, S.Y.; Ye, D.; Chen, Y.; Lu, C. Molecular phylogeny of the ant subfamily Formicinae (Hymenoptera, Formicidae) from China based on mitochondrial genes. Sociobiology 2013, 60, 135–144. [Google Scholar] [CrossRef] [Green Version]
  104. Park, J.; Xi, H.; Park, J. The complete mitochondrial genome of Aphaenogaster famelica (Smith, 1874) (Hymenoptera: Formicidae). Mitochondrial DNA Part B 2020, 5, 492–494. [Google Scholar] [CrossRef] [Green Version]
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Figure 1. Complete WBPHTA mitochondrial genome sequence. Black circle indicates the WBPHTA mitogenome, yellow bars are protein-coding genes, purple bars are tRNAs, and red bars mean rRNAs. Each gene name was displayed with lines directing to the corresponded bars.
Figure 1. Complete WBPHTA mitochondrial genome sequence. Black circle indicates the WBPHTA mitogenome, yellow bars are protein-coding genes, purple bars are tRNAs, and red bars mean rRNAs. Each gene name was displayed with lines directing to the corresponded bars.
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Insects 12 01066 g002 550
Figure 2. Length variations of the WBPH, SBPH, and BPH complete mitogenomes. (A) present the histogram of all available WBPH, SBPH, and BPH complete mitogenomes. The grey-colored box indicates 75 percentile of mitogenome length and the middle line means the median value of mitogenome length. Small circles indicate outliers. (B) display the histogram of all available WBPH, SBPH, and BPH mitogenomes except the seven BPH mitogenomes which lack their control regions.
Figure 2. Length variations of the WBPH, SBPH, and BPH complete mitogenomes. (A) present the histogram of all available WBPH, SBPH, and BPH complete mitogenomes. The grey-colored box indicates 75 percentile of mitogenome length and the middle line means the median value of mitogenome length. Small circles indicate outliers. (B) display the histogram of all available WBPH, SBPH, and BPH mitogenomes except the seven BPH mitogenomes which lack their control regions.
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Insects 12 01066 g003 550
Figure 3. Identification and validation of polymorphic site on WBPHTA mitogenome. (A) presents the alignment of NGS raw reads around the polymorphic site on the WBPHTA mitogenome (4667 bp). Consensus bases were displayed as colored base characters. Assembled mitogenome sequences were presented with coordination and coded amino acids. NGS raw reads aligned against the assembled mitogenome were displayed under the assembled mitogenome sequences. The block-dotted box indicates the polymorphic site. (B) exhibited sequencing depth around the heteroplasmy site (4667th). The X-axis indicates coordination of mitogenome and Y-axis presented sequencing depth as log scale. (C) shows the alignment of sequencing chromatograms against the WBPHTA mitogenome. Labels at the left side indicate sample name (SF plus number) and sequencing direction (FWD; forward and REV; reverse) together. The block-dotted box indicates the polymorphic site.
Figure 3. Identification and validation of polymorphic site on WBPHTA mitogenome. (A) presents the alignment of NGS raw reads around the polymorphic site on the WBPHTA mitogenome (4667 bp). Consensus bases were displayed as colored base characters. Assembled mitogenome sequences were presented with coordination and coded amino acids. NGS raw reads aligned against the assembled mitogenome were displayed under the assembled mitogenome sequences. The block-dotted box indicates the polymorphic site. (B) exhibited sequencing depth around the heteroplasmy site (4667th). The X-axis indicates coordination of mitogenome and Y-axis presented sequencing depth as log scale. (C) shows the alignment of sequencing chromatograms against the WBPHTA mitogenome. Labels at the left side indicate sample name (SF plus number) and sequencing direction (FWD; forward and REV; reverse) together. The block-dotted box indicates the polymorphic site.
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Insects 12 01066 g004 550
Figure 4. Three-dimensional structure of COX3 with a non-synonymous mutation from heteroplasmy. A three-dimensional structure of COX3 as ribbon type was displayed. The red color indicates amino acid variation identified from the heteroplasmy phenomenon of WBPH mitogenomes. (A) The normal type of COX3; (B) Mutation type of COX3 is caused by the heteroplasmy phenomenon identified in this study.
Figure 4. Three-dimensional structure of COX3 with a non-synonymous mutation from heteroplasmy. A three-dimensional structure of COX3 as ribbon type was displayed. The red color indicates amino acid variation identified from the heteroplasmy phenomenon of WBPH mitogenomes. (A) The normal type of COX3; (B) Mutation type of COX3 is caused by the heteroplasmy phenomenon identified in this study.
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Insects 12 01066 g005 550
Figure 5. Intraspecific variations were identified from the three WBPH mitogenomes. (A) The blue-colored round box indicates WBPHTA mitogenome and two yellow-colored round boxes mean the two previously sequenced WBPH mitogenomes. Numbers of SNPs and INDELs with the total length of INDELs identified from the two WBPH mitogenomes are presented on the lines connected to the boxes. (B) Diagram of the longest INDEL identified among three WBPH mitogenomes.
Figure 5. Intraspecific variations were identified from the three WBPH mitogenomes. (A) The blue-colored round box indicates WBPHTA mitogenome and two yellow-colored round boxes mean the two previously sequenced WBPH mitogenomes. Numbers of SNPs and INDELs with the total length of INDELs identified from the two WBPH mitogenomes are presented on the lines connected to the boxes. (B) Diagram of the longest INDEL identified among three WBPH mitogenomes.
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Insects 12 01066 g006 550
Figure 6. SSR comparison was identified from the three WBPH mitogenomes. (A) The X-axis indicates SSR types and Y-axis shows the number of SSRs. Three colors, blue, orange, and grey, mean the three WBPH mitogenomes, WBPHHN, WBPHYN, and WBPHTA, respectively. (B) Vann diagram displays the classification of SSR groups identified from the three WBPH mitogenomes. Transparent blue-colored, red-colored, and grey-colored circles indicate the mitogenome of WBPHTA, WBPHHN, and WBPHYN, respectively. Numbers on the Vann diagram present a number of SSR groups.
Figure 6. SSR comparison was identified from the three WBPH mitogenomes. (A) The X-axis indicates SSR types and Y-axis shows the number of SSRs. Three colors, blue, orange, and grey, mean the three WBPH mitogenomes, WBPHHN, WBPHYN, and WBPHTA, respectively. (B) Vann diagram displays the classification of SSR groups identified from the three WBPH mitogenomes. Transparent blue-colored, red-colored, and grey-colored circles indicate the mitogenome of WBPHTA, WBPHHN, and WBPHYN, respectively. Numbers on the Vann diagram present a number of SSR groups.
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Insects 12 01066 g007 550
Figure 7. Phylogenetic tree of 32 Delphacidae mitogenomes. Phylogenetic trees constructed by Maximum-Likelihood (ML) and Bayesian inference (BI) methods were presented with supportive values of ML and BI, respectively, on the branches. Accession names and species names were printed on the right side of the phylogenetic tree. Subfamily names were shown with the thick bars at the right side of the tree.
Figure 7. Phylogenetic tree of 32 Delphacidae mitogenomes. Phylogenetic trees constructed by Maximum-Likelihood (ML) and Bayesian inference (BI) methods were presented with supportive values of ML and BI, respectively, on the branches. Accession names and species names were printed on the right side of the phylogenetic tree. Subfamily names were shown with the thick bars at the right side of the tree.
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Table
Table 1. Characteristics of three available WBPH mitogenomes.
Table 1. Characteristics of three available WBPH mitogenomes.
NameLength
(bp)		GC Ratio (%)GC SkewAT SkewAT-Rich Region Length (bp)GC Ratio of AT-Rich Region (%)GenBank Accession NumberReference
WBPHTA16,61323.8−0.141630.094715221917.5MK907866This study
WBPHHN16,61223.8−0.140550.092920222317.5NC_021417[8]
WBPHYN16,65423.8−0.140700.094262226417.7KC512915[8]
Table
Table 2. List of simple sequence repeats (SSRs) identified from a new WBPH mitogenome collected in Korea.
Table 2. List of simple sequence repeats (SSRs) identified from a new WBPH mitogenome collected in Korea.
NoNameSSRTypeTypeStartEndUnit SequenceRepeat #Genes
1M0000001Normal SSRMonoSSR858868A11ND2
2M0000002Normal SSRMonoSSR70447053A10ND5
3M0000003Normal SSRMonoSSR77257737A13ND5
4M0000004Normal SSRMonoSSR78307839A10ND4
5M0000005Normal SSRMonoSSR81108123A14ND4
6M0000006Normal SSRMonoSSR84128421A10ND4
7M0000007Normal SSRMonoSSR87178727A11ND4
8M0000008Normal SSRMonoSSR90579066A10ND4
9M0000009Normal SSRMonoSSR10,02310,032T10
10M0000010Normal SSRMonoSSR10,03310,064A32
11M0000011Normal SSRMonoSSR11,81911,830A12ND1
12M0000012Normal SSRMonoSSR14,55514,569T15
13M0000013Normal SSRMonoSSR14,96614,988T23
14D0000001Normal SSRDiSSR14,78514,796TA6
15D0000002Normal SSRDiSSR14,86214,873TA6
16D0000003Normal SSRDiSSR15,10615,115AT5
17D0000004Normal SSRDiSSR15,14715,160AT7
18D0000005Normal SSRDiSSR15,19215,201AT5
19D0000006Normal SSRDiSSR15,20815,223TA8
20D0000007Normal SSRDiSSR15,24415,253TA5
21D0000008Normal SSRDiSSR15,27415,285TA6
22D0000009Normal SSRDiSSR15,33515,344TA5
23D0000010Normal SSRDiSSR15,38715,396TA5
24T0000001Normal SSRTriSSR15,11715,128ATT4
25Te0000001Normal SSRTetraSSR84438454ATAA3ND4
Table
Table 3. List of simple sequence repeats (SSRs) from SSR groups containing one or two mitogenomes.
Table 3. List of simple sequence repeats (SSRs) from SSR groups containing one or two mitogenomes.
NoSSR Group MitogenomeSSR TypeTypeSSR NameStartEndUnit Sequence# of RepeatsGenes
1SSRGroup 16WBPHHNPotential SSRPentaSSRP000004715,34615,355AATAA2Intergenic
WBPHYNPotential SSRPentaSSRP000004715,34615,355AATAA2Intergenic
2SSRGroup 34WBPHHNNormal SSRMonoSSRM000000910,02310,032T10Intergenic
WBPHTANormal SSRMonoSSRM000000910,02310,032T10Intergenic
3SSRGroup 75WBPHHNPotential SSRPentaSSRP000002310,33310,342TACAC2CYTB
WBPHYNPotential SSRPentaSSRP000002310,33310,342TACAC2CYTB
4SSRGroup 99WBPHYNPotential SSRPentaSSRP000004415,03415,043ATATA2Intergenic
WBPHTAPotential SSRPentaSSRP000004415,03515,044ATATA2Intergenic
5SSRGroup 103WBPHYNPotential SSRHexaSSRH000002110,49810,509TAAAAG2CYTB
WBPHHNPotential SSRHexaSSRH000002110,49810,509TAAAAG2CYTB
6Singleton 1WBPHHNPotential SSRPentaSSRP000002210,01610,025AATTT2Intergenic
7Singleton 2WBPHHNPotential SSRPetanSSRP000004415,03415,043ATATA2Intergenic
8Singleton 3WBPHTAPotential SSRPentaSSRP000002310,33710,346TACAC2Intergenic
9Singleton 4WBPHTAPotential SSRPentaSSRP000004715,34715,356AATAA2Intergenic
10Singleton 5WBPHTAPotential SSRHexaSSRH000002110,50210,513TAAAAG2Intergenic
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Park, J.; Xi, H.; Park, J.; Seo, B.Y. A New Mitochondrial Genome of Sogatella furcifera (Horváth) (Hemiptera: Delphacidae) and Mitogenome-Wide Investigation on Polymorphisms. Insects 2021, 12, 1066. https://doi.org/10.3390/insects12121066

AMA Style

Park J, Xi H, Park J, Seo BY. A New Mitochondrial Genome of Sogatella furcifera (Horváth) (Hemiptera: Delphacidae) and Mitogenome-Wide Investigation on Polymorphisms. Insects. 2021; 12(12):1066. https://doi.org/10.3390/insects12121066

Chicago/Turabian Style

Park, Jongsun, Hong Xi, Jonghyun Park, and Bo Yoon Seo. 2021. "A New Mitochondrial Genome of Sogatella furcifera (Horváth) (Hemiptera: Delphacidae) and Mitogenome-Wide Investigation on Polymorphisms" Insects 12, no. 12: 1066. https://doi.org/10.3390/insects12121066

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