Kinetochore and ionomic adaptation to whole genome duplication

Abstract

Whole genome duplication (WGD) brings challenges to key processes like meiosis, but nevertheless is associated with diversification in all kingdoms. How is WGD tolerated, and what processes commonly evolve to stabilize the new polyploid lineage? Here we study this inCochleariaspp., which have experienced multiple rounds of WGD in the last 300,000 years. We first generate a chromosome-scale genome and sequence 113 individuals from 33 diploid, tetraploid, hexaploid, and outgroup populations. We detect the clearest post-WGD selection signatures in functionally interacting kinetochore components and ion transporters. We structurally model these derived selected alleles, associating them with known WGD-relevant functional variation and compare these results to independent recent post-WGD selection inArabidopsis arenosaandCardamine amara. Some of the same biological processes evolve in all three WGDs, but specific genes recruited are flexible. This points to a polygenic basis for modifying systems that control the kinetochore, meiotic crossover number, DNA repair, ion homeostasis, and cell cycle. Given that DNA management (especially repair) is the most salient category with the strongest selection signal, we speculate that the generation rate of structural genomic variants may be altered by WGD in young polyploids, contributing to their occasionally spectacular adaptability observed across kingdoms.

Impact of whole-genome duplications on structural variant evolution in the plant genusCochlearia

“…tatrae , C. bavarica , and C. polonica ; and octoploid species C. anglica . The tetraploids likely resulted from within-species WGDs (autopolyploids), as evidenced by widespread multivalent formation at meiosis (Bray et al, 2023), whereas the evolutionary history of the higher ploidies is more complex, potentially involving both auto- and allopolyploidisation events. See Koch (2012) and Wolf et al (2021) for comprehensive discussions of the evolutionary history of the Cochlearia species.…”

“…However, due to low sequencing depth, we excluded four diploids from our main analyses (Table S1), resulting in a set of 10 diploids, seven tetraploids, one hexaploid, and one octoploid. After aligning reads against the chromosome build C. excelsa reference genome (Bray et al, 2023), we used Sniffles2 (Smolka et al, 2022) to identify SVs from the alignments. First, as Sniffles2 was developed primarily for diploid organisms, we used simulated data to confirm that it likely has a good power to detect SVs in our high-depth (mean depth = 68) autotetraploid samples (Fig.…”

“…SVs are not only more deleterious than point mutations (Hämälä et al, 2021; Zhou et al, 2019) but also could be more frequently generated in polyploids due more complicated recombination and DNA repair machinery (Bomblies, 2023), as experimentally shown in yeast (Selmecki et al, 2015). Indeed, we previously showed that genes involved in DNA repair have evolved rapidly in the tetraploid C. officinalis since its divergence from the diploid C. pyrenaica (Bray et al, 2023), suggesting that WGD in Cochlearia has resulted in a shift in the (internal) selective environment due to extra challenges in DNA management.…”

“…The fast evolving resistance genes have been associated with SVs in multiple plant species (Bayer et al, 2020), highlighting the importance of structural variation in the ongoing arms race between plants and their pathogens (Anderson et al, 2010). Additionally, SVs have been linked to salinity adaptation in Arabidopsis (Busoms et al, 2018), making SV-mediated adaptation a potential contributor to the high salt tolerance exhibited by these Cochlearia species (Bray et al, 2023; Pegtel, 1999). The Cochlearia species (particularly the diploid C. pyrenaica ) are also highly metallicolous (Nawaz et al, 2017), which could be associated with root development (Dijk et al, 2022) and thus SV-mediated adaptation.…”

“…Here, we focus on populations from the diploid n = 6 species C. pyrenaica, C. excelsa, C. aestuaria, and C. islandica; diploid n = 7 species C. groenlandica and C. triactylites; tetraploid n = 6 species C. officinalis, C. micacea, and C. alpina; hexaploid species C. tatrae, C. bavarica, and C. polonica; and octoploid species C. anglica. The tetraploids likely resulted from within-species WGDs (autopolyploids), as evidenced by widespread multivalent formation at meiosis (Bray et al, 2023), whereas the evolutionary history of the higher ploidies is more complex, potentially involving both auto-and allopolyploidisation events. See Koch (2012) and Wolf et al (2021) for comprehensive discussions of the evolutionary history of the Cochlearia species.…”