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Molecular Evolution of rbcL in Orthotrichales (Bryophyta): Site Variation, Adaptive Evolution, and Coevolutionary Patterns of Amino Acid Replacements

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Abstract

Molecular evolution of the large subunit of the RuBisCO enzyme is understudied in early diverging land plants. These groups show morphological and eco-physiological adaptations to the uneven and intermittent distribution of water in the terrestrial environment. This might have prompted a continuous fine-tuning of RuBisCO under a selective pressure modifying the species-specific optima for photosynthesis in contrasting microdistributions and environmental niches. To gain a better insight into the molecular evolution of RuBisCO large subunits, the aim of this study was to assess the pattern of evolutionary change in the amino acid residues in a monophyletic group of Bryophyta (Orthotrichaceae). Tests for positive, neutral, or purifying selection at the amino acid level were assessed by comparing rates (ω) of non-synonymous (dN) and synonymous (dS) nucleotide substitutions along a Maximum Likelihood phylogenetic tree. Molecular adaptation tests using likelihood ratio tests, reconstruction of ancestral amino acid sites, and intra-protein coevolution analyses were performed. Variable amino acid sites (39) were unevenly distributed across the LSU. The residues are located on rbcL sites that are highly variable in higher plants and close to key regions implying dimer–dimer (L2L2), RuBisCO-activase interactions, and conformational functions during catalysis. Ten rbcL sites (32, 33, 91, 230, 247, 251, 255, 424, 449 and 475) have been identified by the Bayesian Empirical Bayes inference to be under positive selection and under adaptive evolution under the M8 model. The pattern of amino acid variation suggests that it is not lineage specific, but rather representative of a case of convergent evolution, suggesting recurrent changes that potentially favor the same amino acid substitutions that are likely optimized the RuBisCO activity.

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Acknowledgements

We thank the subject editor, two anonymous reviewers, and J. Martínez-Abaigar for providing insightful comments and constructive criticisms that greatly improved the manuscript.

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MB and JAR conceived the study, MB and JAR designed the analysis performance, MB performed the analysis, and MB and JAR wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Josep A. Rosselló.

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The authors declare that they have no conflict of interest.

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All authors declare that they have read and approved the manuscript version to be published.

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Handling editor: Dorothee Huchon.

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Bernabeu, M., Rosselló, J.A. Molecular Evolution of rbcL in Orthotrichales (Bryophyta): Site Variation, Adaptive Evolution, and Coevolutionary Patterns of Amino Acid Replacements. J Mol Evol 89, 225–237 (2021). https://doi.org/10.1007/s00239-021-09998-w

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  • DOI: https://doi.org/10.1007/s00239-021-09998-w

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