Circadian regulation of the transcriptome in a complex polyploid crop

Abstract

The circadian clock is a finely balanced timekeeping mechanism that coordinates programmes of gene expression. It is currently unknown how the clock regulates expression of homoeologous genes in polyploids. Here, we generate a high-resolution time-course dataset to investigate the circadian balance between sets of 3 homoeologous genes (triads) from hexaploid bread wheat. We find a large proportion of circadian triads exhibit imbalanced rhythmic expression patterns, with no specific subgenome favoured. In wheat, period lengths of rhythmic transcripts are found to be longer and have a higher level of variance than in other plant species. Expression of transcripts associated with circadian controlled biological processes is largely conserved between wheat and Arabidopsis; however, striking differences are seen in agriculturally critical processes such as starch metabolism. Together, this work highlights the ongoing selection for balance versus diversification in circadian homoeologs and identifies clock-controlled pathways that might provide important targets for future wheat breeding.

Genome-wide circadian gating of a cold temperature response in bread wheat

“…C-repeat binding factors (CBFs) are well-described cold responsive transcription factors ( 51, 52 ), with up to 25 CBFs present in wheat ( 53 ). Certain CBF transcripts have a circadian rhythm in barley and wheat ( 39, 54 ), and in Arabidopsis the cold-induction of CBFs is gated by the circadian clock ( 28 ). Our data indicate that circadian gating of CBF cold-responsiveness is conserved in wheat and can extend across homoeolog triads, such as for TaCBFIVc-B14 , which is a cold-responsive CBF ortholog with high homology to AtCBF2 (Fig.…”

“…A range of related Arabidopsis transcripts encoding starch degradation enzymes are circadian regulated, but this is not always conserved in wheat, where certain orthologs of β-amylase (BAM, e.g. BAM3 ) have a circadian rhythm, whereas BAM1 does not ( 39 ). Under our conditions, TaBAM1 triad and TaBAM3 triad were cold-responsive during the subjective day (Fig.…”

“…The wheat subgenomes arose from hybridisation of three diploid ancestors, resulting in a circadian oscillator that likely incorporates more components than diploid species. No specific subgenome is favoured across the circadian regulated transcriptome of wheat ( 39 ), although circadian regulated paralogs have differential expression patterns in other crops ( 44 ). Furthermore, environmentally-responsive gene triads do not always have expression that is balanced across the subgenomes ( 46 ).…”

“…Circadian clock gene loci such as TaPpd (orthologous to Arabidopsis PRR3 or PRR7) determine agriculturally-important photoperiod responses of domesticated wheat (40)(41)(42)(43). The complexity of this signal integration is increased in polyploid crops such as wheat by the presence of multiple gene paralogs or homoeologs that can have differential patterns of circadian regulation (39,44). In hexaploid wheat, over 50% of genes (approximately 50,000 genes) occur as sets of three gene homoeologs termed triads (45,46), providing an informative genomic structure to study environmentally-responsive gene expression within polyploid genomes.…”

The wheat clock strikes a balance across subgenomes to regulate gene expression

“…Our understanding of the plant clock is primarily from work in the model dicot plant Arabidopsis thaliana. With many major crops being monocots, a recent study [6] set out to characterize the circadian transcriptome of the bread wheat Triticum aestivum, one of the most important and widely grown crops globally. Roughly one-third of expressed genes were classified as clock regulated in T. aestivum with period lengths longer and with a higher variance than Arabidopsis, Brassica rapa (field mustard), Glycine max (soybean), and Brachypodium distachyon (temperate grass model), suggesting that circadian clock features in wheat are distinct.…”