Gradual evolution of allopolyploidy in Arabidopsis suecica

Robin Burns,Terezie Mandáková,Luz Mayela Soto-Jiménez,Martin A Lysak,Polina Yu Novikova,Magnus Nordborg,Chang Liu,Joanna Gunis

doi:10.1038/s41559-021-01525-w

Abstract

Most diploid organisms have polyploid ancestors. The evolutionary process of polyploidization is poorly understood but has frequently been conjectured to involve some form of ‘genome shock’, such as genome reorganization and subgenome expression dominance. Here we study polyploidization in Arabidopsis suecica, a post-glacial allopolyploid species formed via hybridization of Arabidopsis thaliana and Arabidopsis arenosa. We generated a chromosome-level genome assembly of A. suecica and complemented it with polymorphism and transcriptome data from all species. Despite a divergence around 6 million years ago (Ma) between the ancestral species and differences in their genome composition, we see no evidence of a genome shock: the A. suecica genome is colinear with the ancestral genomes; there is no subgenome dominance in expression; and transposon dynamics appear stable. However, we find changes suggesting gradual adaptation to polyploidy. In particular, the A. thaliana subgenome shows upregulation of meiosis-related genes, possibly to prevent aneuploidy and undesirable homeologous exchanges that are observed in synthetic A. suecica, and the A. arenosa subgenome shows upregulation of cyto-nuclear processes, possibly in response to the new cytoplasmic environment of A. suecica, with plastids maternally inherited from A. thaliana. These changes are not seen in synthetic hybrids, and thus are likely to represent subsequent evolution.

Highlights

Ancient polyploidization or whole-genome duplication is a hallmark of most higher-organism genomes[1,2], including our own[3,4]
We focus on an allopolyploid comparable in age to these examples: the highly selfing[72] A. suecica, which was formed through the hybridization of A. thaliana and A. arenosa around 16 thousand years ago, during the Last Glacial Maximum[20], and which is currently found in northern Fennoscandia (Fig. 1a)
This study has focused on the process of polyploidization in a natural allotetraploid species, A. suecica

Summary

Introduction

Ancient polyploidization or whole-genome duplication is a hallmark of most higher-organism genomes[1,2], including our own[3,4] While most of these organisms are diploid and show only traces of polyploidy, there are many examples of recent polyploidization, especially among flowering plants[5,6,7,8,9]. 73), and based on organelle sequences, A. thaliana is the maternal and A. arenosa is the paternal parent[74] This scenario is supported by A. arenosa being a ploidy-variable species, such that A. suecica could readily be generated by the fusion of an unreduced A. thaliana egg cell and an autotetraploid A. arenosa sperm cell[20,75]. Our main goal was to look for evidence of genome changes ( the kind of dramatic changes discussed above) in A. suecica relative to the ancestral species

Methods

Results

Conclusion