Whole genome duplication is widespread in plant evolutionary history and is followed by non-random gene loss to return to a diploid state. Across multiple angiosperm species, the retained genes tend to be dosage-sensitive regulatory genes such as transcription factors, yet data for younger polyploid species is sparse. Here we analysed the retention, expression and genetic variation in transcription factors in the recent allohexaploid bread wheat (Triticum aestivum L.). By comparing diploid, tetraploid and hexaploid wheats we found that, following each of two hybridisation and whole genome duplication events, the proportion of transcription factors in the genome increased. Transcription factors were preferentially retained over other genes as homoeologous groups in tetraploid and hexaploid wheat. Across cultivars, transcription factor homoeologs contained fewer deleterious missense mutations than non-transcription factors, suggesting that transcription factors are maintained as three functional homoeologs in hexaploid wheat populations. Transcription factor homoeologs were more strongly co-expressed than non-transcription factors, indicating conservation of function between homoeologs. We found that the B3, MADS-M-type and NAC transcription factor families were less likely to have three homoeologs present than other families, which was associated with low expression levels and high levels of tandem duplication. Together, our results show that transcription factors are preferentially retained in polyploid wheat genomes although there is variation between families. Knocking out one transcription factor homoeolog to alter gene dosage, using TILLING or CRISPR, could generate new phenotypes for wheat breeding.
Whole genome duplication (WGD) is widespread in plant evolutionary history, but the mechanisms of non-random gene loss after WGD are debated. The gene balance hypothesis proposes that dosage-sensitive genes such as regulatory genes are retained in polyploids. To test this hypothesis, we analysed the retention of transcription factors (TFs) in the recent allohexaploid bread wheat (Triticum aestivum). We annotated TFs in hexaploid, tetraploid and diploid wheats; compared the co-expression of homoeologous TF and non-TF triads; and analysed single nucleotide variation in TFs across cultivars. We found that, following each of two hybridisation and WGD events, the proportion of TFs in the genome increased. TFs were preferentially retained over other genes as homoeologous groups in tetraploid and hexaploid wheat. Across cultivars, TF triads contain fewer deleterious missense mutations than non-TFs. TFs are preferentially retained as three functional homoeologs in hexaploid wheat, in support of the gene balance hypothesis. High co-expression between TF homoeologs suggests that neo- and sub-functionalisation are not major drivers of TF retention in this young polyploid. Knocking out one TF homoeolog to alter gene dosage, using TILLING or CRISPR, could be a way to further test the gene balance hypothesis and generate new phenotypes for wheat breeding.
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