Evolutionary divergence of duplicated genomes in newly described allotetraploid cottons

Abstract

Allotetraploid cotton (<i>Gossypium</i>) species represents a model system for the study of plant polyploidy, molecular evolution, and domestication. Here, chromosome-scale genome sequences were obtained and assembled for two recently described wild species of tetraploid cotton, <i>Gossypium ekmanianum</i> [(AD)₆, <i>Ge</i>] and <i>Gossypium stephensii</i> [(AD)₇, <i>Gs</i>], and one early form of domesticated <i>Gossypium hirsutum</i>, race <i>punctatum</i> [(AD)₁, <i>Ghp</i>]. Based on phylogenomic analysis, we provide a dated whole-genome level perspective for the evolution of the tetraploid <i>Gossypium</i> clade and resolved the evolutionary relationships of <i>Gs</i>, <i>Ge</i>, and domesticated <i>G. hirsutum</i>. We describe genomic structural variation that arose during <i>Gossypium</i> evolution and describe its correlates-including phenotypic differentiation, genetic isolation, and genetic convergence-that contributed to cotton biodiversity and cotton domestication. Presence/absence variation is prominent in causing cotton genomic structural variations. A presence/absence variation-derived gene encoding a phosphopeptide-binding protein is implicated in increasing fiber length during cotton domestication. The relatively unimproved <i>Ghp</i> offers the potential for gene discovery related to adaptation to environmental challenges. Expanded gene families enoyl-CoA δ isomerase 3 and RAP2-7 may have contributed to abiotic stress tolerance, possibly by targeting plant hormone-associated biochemical pathways. Our results generate a genomic context for a better understanding of cotton evolution and for agriculture.