| Abstract | INTRODUCTION: Polyploidy, arising from whole-genome duplication or interspecific hybridization, is ubiquitous across the plant and fungal kingdoms. The presence of highly related genes in polyploids, referred to as homoeologs, has been proposed to confer adaptive plasticity—for example, through neofunctionalization of duplicated genes or tissue-specific expression. This plasticity has facilitated the domestication and adaptation of major polyploid crops (e.g., wheat, cotton, and coffee). However, despite its likely importance, we have a limited understanding of the effect of polyploidy on gene expression and the extent to which homoeologs are similar or different in their expression patterns across development and tissues. RATIONALE: Bread wheat is a polyploid derived from the hybridizations between three distinct diploid species and is an informative system for analyzing the effects of recent polyploidy on gene expression. Understanding the coordination of homoeologs and identifying the mechanisms associated with these processes should help define strategies to improve trait biology in a crop that provides more than 20% of the protein and caloric intake of humans. RESULTS: Here we leverage 850 wheat RNA-sequencing samples, alongside the annotated genome, to determine the similarities and differences between homoeolog expression across a range of tissues, developmental stages, and cultivars. On average, ~30% of wheat homoeolog triads (composed of A, B, and D genome copies) showed nonbalanced expression patterns, with higher or lower expression from a single homoeolog with respect to the other two. These differences between homoeologs were associated with epigenetic changes affecting DNA methylation and histone modifications. Although nonbalanced homoeolog expression could be partially predicted by expression in diploid ancestors, large changes in relative homoeolog expression were observed owing to polyploidization. Our results suggest that the transposable elements in promoters relate more closely to the variation in the relative expression of homoeologs across tissues than to a ubiquitous effect across all tissues. We found that homoeologs with the highest inter-tissue variation had promoters with more frequent transposable element insertions and more varied cis-regulatory elements than homoeologs that were stable across tissues. We also identified expression asymmetry along wheat chromosomes. Homoeologs with the largest inter-tissue, inter-cultivar, and coding sequence variation were most often located in the highly recombinogenic distal ends of chromosomes. These transcriptionally dynamic homoeologs are under more relaxed selection pressure, potentially representing the first steps toward functional innovation through neo- or subfunctionalization. We generated tissue- and stress-specific coexpression networks that reveal extensive coordination of homoeolog expression throughout development. These networks, alongside detailed gene expression atlases (www.wheat-expression.com and http://bar.utoronto.ca), lay the groundwork to identify candidate genes influencing agronomic traits in wheat. CONCLUSION: This study provides detailed insights into the transcriptional landscape of bread wheat, an evolutionarily young polyploid. Our work shows that homoeolog expression patterns in bread wheat have been shaped by polyploidy and are associated with both epigenetic modifications and variation in transposable elements within promoters of homoeologous genes. The extensive datasets and analyses presented here provide a framework that can help researchers and breeders develop strategies to improve crops by manipulating individual or multiple homoeologs to modulate trait responses. |
|---|
