Effects of homoeologous exchange on gene expression and alternative splicing in a newly formed allotetraploid wheat

Plant J. 2022 Jun 28. doi: 10.1111/tpj.15886. Online ahead of print.

Abstract

Homoeologous exchange (HE) is a major mechanism generating post-polyploidization genetic variation with important evolutionary consequences. However, the direct impacts of HE on gene expression and transcript diversity in allopolyploids without the intertwined evolutionary processes remain to be fully understood. Here, we analyzed high-throughput RNA-seq data of young leaves from plant groups of a synthetic allotetraploid wheat (AADD), which contained variable numbers of HEs. We aimed to investigate if and to which extent HE directly impacts gene expression and alternative splicing (AS). We found that HE impacts expression of genes located within HE regions primarily via a cis-acting dosage effect, which led to significant changes in the total expression level of homoeologous gene pairs, especially for homoeologs whose original expression was biased. In parallel, HE also influences expression of a large number of genes residing in non-HE regions by trans-regulation leading to convergent expression of homoeologs. Intriguingly, when taking the original relative homoeolog expression states into account, homoeolog pairs under trans-effect are more prone to manifesting a convergent response to the HEs whereas those under cis-regulation tended to show further exacerbated subgenome-biased expression. Moreover, HE-induced quantitative, largely individual-specific, changes of AS events were detected. Similar to homoeologous expression, homoeo-AS events under trans-effect were more responsive to HE. HE therefore exerts multifaceted immediate effects on gene expression and, to a less extent, on individualized transcript diversity in nascent allopolyploidy.

Keywords: alternative splicing; gene expression; homoeologous exchange; synthetic wheat.