Abstract
Cis and trans regulatory divergence underlies phenotypic and evolutionary diversification. Relatively little is understood about the complexity of regulatory evolution accompanying crop domestication, particularly for polyploid plants. Here, we compare the fiber transcriptomes between wild and domesticated cotton (Gossypium hirsutum) and their reciprocal F1 hybrids, revealing genome-wide (~15%) and often compensatory cis and trans regulatory changes under divergence and domestication. The high level of trans evolution (54%–64%) observed is likely enabled by genomic redundancy following polyploidy. Our results reveal that regulatory variation is significantly associated with sequence evolution, inheritance of parental expression patterns, co-expression gene network properties, and genomic loci responsible for domestication traits. With respect to regulatory evolution, the two subgenomes of allotetraploid cotton are often uncoupled. Overall, our work underscores the complexity of regulatory evolution during fiber domestication and may facilitate new approaches for improving cotton and other polyploid plants.
Highlights
Cis and trans regulatory divergence underlies phenotypic and evolutionary diversification
The first-generation intra- and interspecific hybrids have been used for analyses of allele-specific expression (ASE), which isolate expression changes attributed to cis regulatory divergence between the parents, thereby facilitating observation of trans effects that are shared in the hybrid[13]
One interesting and relevant feature of the allopolyploid genome is that its two subgenomes differ two-fold in size despite having approximately the same number of genes; this raises the prospect that polyploidy was accompanied by the merger of two rather different cis/trans regulatory systems, which subsequently have been shaped by natural evolution[24]
Summary
Cis and trans regulatory divergence underlies phenotypic and evolutionary diversification. Often combined with fine-mapping and, more recently, comparative population genomics approaches, have led to significant progress in identifying causative genetic changes that underlie domestication traits These studies provide multiple examples of specific coding sequence variants (SNP/indel polymorphisms, amino acid substitutions, mis-splice mutations, transposon insertions) that have increased in frequency or been fixed by strong directional human selection[4,5,6]. One spectacular example is the teosinte branched 1 (tb1) gene in maize, where selection (from standing variation) for overexpression, mediated by a transposon insertion, caused an increase in apical dominance during domestication of maize from its ancestor, teosinte[9] This and other examples highlight the prominence of regulatory evolution in the origin of new phenotypes under domestication, and by extension, in natural settings as well[10,11]. We further explore the potential functions of relevant genes to fiber morphology in the context of gene co-expression and regulatory networks
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