Evolution of the beta-amylase gene in the temperate grasses: Non-purifying selection, recombination, semiparalogy, homeology and phylogenetic signal

• Published in: Molecular phylogenetics and evolution Vol. 91; pp. 68 - 85
• Main Authors: Minaya, Miguel, Díaz-Pérez, Antonio, Mason-Gamer, Roberta, Pimentel, Manuel, Catalán, Pilar
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.10.2015
• Subjects: allopolyploidy; beta-amylase; beta-Amylase - classification; beta-Amylase - genetics; clones; concerted evolution; Evolution, Molecular; Festuca; gene conversion; genes; Genes, Plant; Genetic Markers; grasses; internal transcribed spacers; Introns; Low copy nuclear genes; mutation; Phylogenetic incongruence; Phylogeny; Poaceae - classification; Poaceae - genetics; Pooideae; Pseudogenes; Pseudogenization; Purifying and diversifying selection; Recombination, Genetic; ribosomal DNA; Selection, Genetic; Vulpia alopecuros; β-amylase phylogeny; Low copy nuclear genes; Phylogenetic incongruence; Pooideae; Pseudogenization; Purifying and diversifying selection; β-amylase phylogeny
• ISSN: 1055-7903; 1095-9513; 1095-9513
• DOI: 10.1016/j.ympev.2015.05.014

[Display omitted] •Pseudogenes and recombinants were detected in β-amylase sequences of grasses.•Potential paralogy was found in the diploid Vulpia alopecurus clones.•A homeologous β-amylase copy supports a Mahgrebian-Schedonorus paternal parent of Festuca simensis.•The β-amylase gene reconstructs a plausible grass phylogeny when the discordant and other atypical sequences are removed. Low-copy nuclear genes (LCNGs) have complex genetic architectures and evolutionary dynamics. However, unlike multicopy nuclear genes, LCNGs are rarely subject to gene conversion or concerted evolution, and they have higher mutation rates than organellar or nuclear ribosomal DNA markers, so they have great potential for improving the robustness of phylogenetic reconstructions at all taxonomic levels. In this study, our first objective is to evaluate the evolutionary dynamics of the LCNG β-amylase by testing for potential pseudogenization, paralogy, homeology, recombination, and phylogenetic incongruence within a broad representation of the main Pooideae lineages. Our second objective is to determine whether β-amylase shows sufficient phylogenetic signal to reconstruct the evolutionary history of the Pooid grasses. A multigenic (ITS, matK, ndhF, trnTL, and trnLF) tree of the study group provided a framework for assessing the β-amylase phylogeny. Eight accessions showed complete absence of selection, suggesting putative pseudogenic copies or other relaxed selection pressures; resolution of Vulpia alopecuros 2x clones indicated its potential (semi) paralogy; and homeologous copies of allopolyploid species Festuca simensis, F. fenas, and F. arundinacea tracked their Mediterranean origin. Two recombination events were found within early-diverged Pooideae lineages, and five within the PACCMAD clade. The unexpected phylogenetic relationships of 37 grass species (26% of the sampled species) highlight the frequent occurrence of non-treelike evolutionary events, so this LCNG should be used with caution as a phylogenetic marker. However, once the pitfalls are identified and removed, the phylogenetic reconstruction of the grasses based on the β-amylase exon+intron positions is optimal at all taxonomic levels.