Song Qingxin, Zhang Tianzhen, Stelly David M, Chen Z Jeffrey
Department of Molecular Biosciences, Institute for Cellular and Molecular Biology, and Center for Computational Biology and Bioinformatics, The University of Texas at Austin, Austin, TX, 78712, USA.
State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, 210095, China.
Genome Biol. 2017 May 31;18(1):99. doi: 10.1186/s13059-017-1229-8.
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. However, the relationship between DNA methylation and polyploid plant domestication remains elusive.
We 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.
We 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.
多倍体是所有开花植物和一些动物普遍存在的进化特征，会导致影响基因表达和形态的遗传和表观遗传变化。DNA甲基化变化可产生减数分裂稳定的表观等位基因，这些等位基因可通过选择和育种进行传递。然而，DNA甲基化与多倍体植物驯化之间的关系仍不明确。
我们报告了全面的表观基因组和功能分析，包括在驯化的异源四倍体棉花及其四倍体和二倍体亲属中约1200万个差异甲基化的胞嘧啶。甲基化基因的进化速度比未甲基化基因快；同源位点之间的DNA甲基化变化与异源四倍体中的同源基因表达偏向有关。值得注意的是，种间杂种中诱导的甲基化变化在很大程度上在异源四倍体中得以维持。在野生棉和栽培棉之间鉴定出的519个差异甲基化基因中，有些基因有助于驯化性状，包括开花时间和种子休眠。CONSTANS（CO）和CO-LIKE（COL）基因调节拟南芥的光周期。COL2是异源四倍体棉花中的一个表观等位基因。COL2A高度甲基化并沉默，而COL2D在野生棉中受到抑制，但在所有测试的驯化棉中由于甲基化缺失而高度表达。抑制DNA甲基化会激活COL2的表达，而在栽培棉中抑制COL2会延迟开花。
我们揭示了棉花进化过程中驯化性状的表观基因组特征。COL2的去甲基化增加了其表达，诱导光周期开花，这可能有助于棉花在全球范围内的种植适应性。这些资源应有助于多倍体作物的表观遗传工程、育种和改良。
