Abstract
BackgroundPolyploidy is a pervasive evolutionary feature of all flowering plants and some animals, leading to genetic and epigenetic changes that affect gene expression and morphology. DNA methylation changes can produce meiotically stable epialleles, which are transmissible through selection and breeding. However, the relationship between DNA methylation and polyploid plant domestication remains elusive.ResultsWe report comprehensive epigenomic and functional analyses, including ~12 million differentially methylated cytosines in domesticated allotetraploid cottons and their tetraploid and diploid relatives. Methylated genes evolve faster than unmethylated genes; DNA methylation changes between homoeologous loci are associated with homoeolog-expression bias in the allotetraploids. Significantly, methylation changes induced in the interspecific hybrids are largely maintained in the allotetraploids. Among 519 differentially methylated genes identified between wild and cultivated cottons, some contribute to domestication traits, including flowering time and seed dormancy. CONSTANS (CO) and CO-LIKE (COL) genes regulate photoperiodicity in Arabidopsis. COL2 is an epiallele in allotetraploid cottons. COL2A is hypermethylated and silenced, while COL2D is repressed in wild cottons but highly expressed due to methylation loss in all domesticated cottons tested. Inhibiting DNA methylation activates COL2 expression, and repressing COL2 in cultivated cotton delays flowering.ConclusionsWe uncover epigenomic signatures of domestication traits during cotton evolution. Demethylation of COL2 increases its expression, inducing photoperiodic flowering, which could have contributed to the suitability of cotton for cultivation worldwide. These resources should facilitate epigenetic engineering, breeding, and improvement of polyploid crops.
Highlights
Polyploidy is a pervasive evolutionary feature of all flowering plants and some animals, leading to genetic and epigenetic changes that affect gene expression and morphology
Integrating the data of methylomes with transcriptomes, we discovered more than 500 putative epialleles that may contribute to morphological and physiological changes during evolution and domestication of polyploid cottons
We further examined whether hybridization-induced methylation changes could be maintained during evolution, compared to polyploidization of allotetraploid cottons that had diverged into five or more different species [34]
Summary
Polyploidy is a pervasive evolutionary feature of all flowering plants and some animals, leading to genetic and epigenetic changes that affect gene expression and morphology. DNA methylation changes can produce meiotically stable epialleles, which are transmissible through selection and breeding. The relationship between DNA methylation and polyploid plant domestication remains elusive. Polyploidy or whole genome duplication (WGD) is a pervasive evolutionary feature of some animals and all flowering plants [1, 2], leading to genetic and epigenetic changes that affect gene expression and morphology [3,4,5]. DNA methylation changes are associated with expression of homoeologous genes in resynthesized and natural Arabidopsis allotetraploids [26,27,28], natural Spartina allopolyploids [29], and paleopolyploid beans [30]. Epigenomic resources in polyploids are very limited, and the functional role of epialleles in morphological evolution and crop domestication remains largely unknown
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