Genome diploidization associates with cladogenesis, trait disparity, and plastid gene evolution

Abstract

Angiosperm genome evolution was marked by many clade-specific whole-genome duplication (WGD) events. The Microlepidieae is one of the monophyletic clades in the mustard family (Brassicaceae) formed after an ancient allotetraploidization. Post-polyploid cladogenesis has resulted in the extant c. 17 genera and 60 species endemic to Australia and New Zealand (10 species). As post-polyploid genome diploidization is a trial-and-error process under natural selection, it may proceed with different intensity and be associated with speciation events. In Microlepidieae, different extents of homoeologous recombination between the two parental subgenomes generated clades marked by slow (“cold”) vs. fast (“hot”) genome diploidization. To gain a deeper understanding of post-polyploid genome evolution in Microlepidieae, we analyzed phylogenetic relationships in this tribe using complete chloroplast sequences, entire 35S rDNA units, and abundant repetitive sequences. The four recovered intra-tribal clades mirror the varied diploidization of Microlepidieae genomes, suggesting that the intrinsic genomic features underlying the extent of diploidization are shared among genera and species within one clade. Nevertheless, even congeneric species may exert considerable morphological disparity (e.g., in fruit shape), whereas some species within different clades experience extensive morphological convergence despite the different pace of their genome diploidization. We showed that faster genome diploidization is positively associated with mean morphological disparity and evolution of chloroplast genes (plastid-nuclear genome coevolution). Higher speciation rates in perennials than in annual species were observed. Altogether, our results confirm the potential of Microlepidieae as a promising subject for the analysis of post-polyploid genome diploidization in Brassicaceae.

Genome assembly of the Brassicaceae diploid Orychophragmus violaceus reveals complex whole-genome duplication and evolution of dihydroxy fatty acid metabolism

“…Polyploidization in higher plants is frequently associated with adaptation and diversification ( Zuo et al., 2022 ). The seed oil of O. violaceus has unique diOH-FAs, and to date, only several related genes have been identified, some of which are dual-function proteins ( Li et al., 2018 ).…”

The evolution of the hypotetraploid Catolobus pendulus genome – the poorly known sister species of Capsella

“…Similar to Catolobus , EET-based descending dysploidy has been documented as a diploidization mechanism in a number of polyploid crucifer taxa, e.g., in Cardamine cordifolia ( Mandáková et al., 2016 ), Microlepidieae ( Mandáková et al., 2010a ; Mandáková et al., 2010b ), or in Pugionium ( Hu et al., 2021 ). Because the pace of chromosomal diploidization can vary even within a single polyploid clade (e.g., Mandáková et al., 2017 ; Mandáková and Lysak, 2018 ; Zuo et al., 2022 ), it is quite difficult to establish credible relationships between the age of polyploid genomes and the pace and extent of their diploidization. However, the dated phylogenetic trees and comparison of polyploid Catolobus and Capsella genomes allow us to draw some conclusions with relative confidence.…”

Polyploid plants take cytonuclear perturbations in stride

“…These taxa exhibit much stronger genome-wide signatures of selection on cytonuclear interactions (Zhang et al, 2015;Havird et al, 2017;Forsythe et al, 2021) that are more akin to observations in animals (Barreto et al, 2018;Yan et al, 2019). Therefore, variation in rates of mitochondrial and plastid sequence evolution across lineages may be an important determinant of selection on N-mt and N-pt genes following polyploidy events (Zuo et al, 2022).…”