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Evolutionary study on the origins of rheophytic goldenrod (Solidago yokusaiana: Asteraceae) with genome and transcriptome analyses

Kyan Ryuta 東北大学

2022.03.25

概要

Understanding adaptation mechanisms is one of most important issues in evolutionary biology. Convergent adaptation provides good opportunities to investigate adaptive evolution. Ecotype pairs, which are sets of populations of same species or closely related ones showing contrasting ecological characters, can be possible natural replicates of convergent adaptation.

 Rheophytes are riparian plants that are adapted and confined to frequently flooded riversides. The rheophytic phenotype has parallelly evolved in different phylogenetic groups and has convergent phenotypic traits, such as narrow leaves, thicker roots, and tough and flexible stems. These traits seem adaptive to flood; therefore, ecotype pair of a rheophyte and its ancestral species is one of representative natural replicates in contrasting environments and will provide a suitable model system for studying convergent adaption.

 The goldenrod species Solidago virgaurea (Asteraceae) is a perennial herb that is widely distributed in Eurasia. In the Japanese Archipelago, the S. virgaurea complex is extremely divergent ecologically and morphologically. Solidago yokusaiana, a rheophytic congener of S. virgaurea, is endemic to Japan, is distributed from Tohoku to Okinawa Districts.

 In chapter I, I examined the parallel origins of S. yokusaiana by distinguishing between multiple and single origins with subsequent gene flow between S. yokusaiana and its progenitor S. virgaurea to confirm convergent adaptation. Some chloroplast haplotypes were shared between S. yokusaiana and S. virgaurea. Also, the population genetic structures revealed by nSSR and SNPs did not correspond to the taxonomic species. The demographic modelling supported the multiple origins of S. yokusaiana in at least four districts and rejected a single origin with ongoing gene flow between the two species, suggesting that S. yokusaiana independently and repeatedly adapted to frequently flooding riversides (Kyan et al., 2021).

 The Japanese S. virgaurea complex may have expanded its range to the Japanese Archipelago during the last glacial period, and S. yokusaiana may have diverged from its progenitor after the last glacial maximum. Considering that the demographic analyses indicated multiple origins in at least four districts, and that the populations of S. yokusaiana have common rheophytic traits, it seems unlikely that the S. yokusaiana in each district evolved via independent de novo mutations after the last glacial maximum, because it is implausible that adaptive mutations arouse at loci related to rheophytic traits in multiple districts in a relatively short period. Therefore, independent selection from the standing genetic variation may have mainly caused the multiple origins of S. yokusaiana. Since mechanisms of the multiple origins are not mutually exclusive, some rheophytic traits or adaptive alleles possibly stemmed from other mechanisms. In addition, because mechanisms causing the multiple origins may also differ in scales of time or space, further studies on loci under divergent selection between the species are needed to elucidate the origins of the rheophytic traits of S. yokusaiana.

 In chapter II, I examined what levels of the genetic hierarchy in which rheophytic convergence have occurred to elucidate the adaptation mechanisms of rheophytism of S. yokusaiana. I compared the gene expression patterns of rheophytic S. yokusaiana and terrestrial S. virgaurea in two districts where both species were sampled. Differentially expressed genes (DEGs) in S. yokusaiana did not show convergence as a whole, and enriched biological functions of the DEGs were more similar between the two districts than the DEGs, suggesting that convergent adaptation of S. yokusaiana in the two districts mainly occurred at a level of the biological functions or their downstream.

 The biological functions specific to S. yokusaiana, which were shared among the two districts were mainly related to DNA replication, suggesting that rheophytism of S. yokusaiana are caused by accelerated cell proliferation through the enriched functions. To regulate species specific leaves size, some mechanisms must coordinate the number and size of leaf cells, and SPL gene family is known to compensate the increased number of cells with decreased size of cells. Also, narrow leaves found commonly in rheophytes were caused by a decreased number of cells in angiosperms and altered cell-elongation process in fern. Therefore, the enriched functions related to DNA replication might be a consequence of the compensation. Considering that functions directly related to cell proliferation were not enriched, endoreduplication, a modified cell cycle lacking mitosis, might contribute to the narrow leaf development, because it contributes to the relationship between the number and size of cells. Furthermore, endoreduplication, which could shorten time and cost of cytokinesis, seems adaptive to environments requiring rapid development, due to frequently disturbed riparian environment.

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