Exceptionally high rates of positive selection on the rbcL gene in the genus Ilex (Aquifoliaceae)

Abstract

BackgroundThe genus Ilex (Aquifoliaceae) has a near-cosmopolitan distribution in mesic habitats from tropical to temperate lowlands and in alpine forests. It has a high rate of hybridization and plastid capture, and comprises four geographically structured plastid groups. A previous study showed that the plastid rbcL gene, coding for the large subunit of Rubisco, has a particularly high rate of non-synonymous substitutions in Ilex, when compared with other plant lineages. This suggests a strong positive selection on rbcL, involved in yet unknown adaptations. We therefore investigated positive selection on rbcL in 240 Ilex sequences from across the global range.ResultsThe rbcL gene shows a much higher rate of positive selection in Ilex than in any other plant lineage studied so far (> 3000 species) by tests in both PAML and SLR. Most positively selected residues are on the surface of the folded large subunit, suggesting interaction with other subunits and associated chaperones, and coevolution between positively selected residues is prevalent, indicating compensatory mutations to recover molecular stability. Coevolution between positively selected sites to restore global stability is common.ConclusionsThis study has confirmed the predicted high incidence of positively selected residues in rbcL in Ilex, and shown that this is higher than in any other plant lineage studied so far. The causes and consequences of this high incidence are unclear, but it is probably associated with the similarly high incidence of hybridization and introgression in Ilex, even between distantly related lineages, resulting in large cytonuclear discordance in the phylogenies.

Dissection for Floral Micromorphology and Plastid Genome of Valuable Medicinal Borages Arnebia and Lithospermum (Boraginaceae)

“…and reported positive selection in most land plants but not in algae and cyanobacteria. A similar study supported the positive selection of rbcL in Ilex using 240 Ilex sequences (Yao et al, 2019). Positive selection in the chloroplast genome, including at rbcL, has been reported in numerous plant taxa (Bock et al, 2014).…”

“…Most genes in the Boraginaceae exhibited stable gene evolution (purifying selection). Positive selection was detected in rbcL, a gene encoding the large subunit of Rubisco, which is commonly observed in angiosperm cp genomes due to the elevated selective pressure for this protein (Kapralov and Filatov, 2007;Shi et al, 2019;Yao et al, 2019). Large-scale studies confirmed that positive selection of rbcL is widespread among land plants.…”

Extremely low nucleotide diversity among thirty-six new chloroplast genome sequences fromAldama(Heliantheae, Asteraceae) and comparative chloroplast genomics analyses with closely related genera

“…Positive selection for rbcL is widespread among land plants ( Kapralov & Filatov, 2007 ; Yao et al, 2019 ; Shen et al, 2020 ) and several studies have demonstrated that positive selection on specific amino-acids in rubisco is linked to plant adaptation to different environmental stresses, facilitating adaptive radiation into diverse ecological niches ( Hermida-Carrera et al, 2017 ). Examples include adaptations to dry or wet climates ( Kapralov & Filatov, 2006 ; Galmés et al, 2014 ), to high altitude environments ( Hu et al, 2015 ) and in transitions from C 3 to C 4 photosynthesis ( Christin et al, 2008 ; Kapralov, Smith & Filatov, 2012 ; Hermida-Carrera et al, 2020 ), including in Flaveria (Asteraceae, tribe Tageteae) ( Kapralov et al, 2011 ).…”

Implications of rbcL and rpoC1 DNA Barcoding in Phylogenetic Relationships of some Egyptian Medicago sativa L. Cultivars

“…Besides that, it assists in comparative studies of population diversity of several plants (Hajibabaei et al, 2007). A high rate of a positive selection among different lineages in Ilex (Aquifoliaceae) was demonstrated (Yao et al, 2019). Amandita et al (2019) has shown that rbcL barcoding has a much higher level of sequence recoverability than matK (95% and 66%, respectively) which in turn have had a great ability to differentiate between flowering plants.…”