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

Abstract

SUMMARY 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.

Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

“…Lloyd et al (2018) found when homoeologous gene pairs have unequal expression, altering the ratio of homoeologous copies does not accurately compensate to maintain the same level of combined homoeolog expression. Similar results have since been observed in tetraploid wheat lines (Zhang et al 2022). Therefore, in the presence of unequal homoeolog expression, HEs will alter the stoichiometry of gene products for a homoeologous pair and would be predicted by the Gene Balance Hypothesis to be under selective constraint to maintain gene dosage balance.…”

Meiotic pairing irregularity and homoeologous chromosome compensation cause rapid karyotype variation in synthetic allotetraploid wheat

“…Moreover, natural allopolyploid species usually possess fully stabilized karyotypes, and hence, there is no real ‘control’ for comparison. By contrast, synthetic allopolyploids are model systems to assess the direct effects and immediate biological consequences of allopolyploidization‐incurred genome shock (Ramsey & Schemske, 2002; Xiong et al ., 2011; Gaebelein et al ., 2019; Ferreira de Carvalho et al ., 2021; Shimizu, 2022; Zhang et al ., 2022). This is because evolution is yet to happen in synthetic allopolyploids, and the same population contains both karyotypically variable and invariable individuals for straightforward comparison.…”

Evaluation of chromosome diversity of Elymus nutans on the Qinghai‐Tibet plateau by FISH

“…Non‐homologous recombination events have been reported in young allopolyploids (e.g. wheat) and may contribute to increasing genetic diversity, thus facilitating the adaptive evolution of newly formed allopolyploids (Zhang et al, 2022). A common non‐homologous recombination is homoeologous exchanges (HEs), which exchange swap pieces of DNA between subgenomes, and can lead to deletions, duplications and translocations (Mason & Wendel, 2020).…”