Allotetraploid cotton is an economically important natural-fiber-producing crop worldwide. After polyploidization, Gossypium hirsutum L. evolved to produce a higher fiber yield and to better survive harsh environments than Gossypium barbadense, which produces superior-quality fibers. The global genetic and molecular bases for these interspecies divergences were unknown. Here we report high-quality de novo-assembled genomes for these two cultivated allotetraploid species with pronounced improvement in repetitive-DNA-enriched centromeric regions. Whole-genome comparative analyses revealed that speciesspecific alterations in gene expression, structural variations and expanded gene families were responsible for speciation and the evolutionary history of these species. These findings help to elucidate the evolution of cotton genomes and their domestication history. The information generated not only should enable breeders to improve fiber quality and resilience to ever-changing environmental conditions but also can be translated to other crops for better understanding of their domestication history and use in improvement.

Summary Xinjiang has been the largest and highest yield cotton production region not only in China, but also in the world. Improvements in Upland cotton cultivars in Xinjiang have occurred via pedigree selection and/or crossing of elite alleles from the former Soviet Union and other cotton producing regions of China. But it is unclear how genomic constitutions from foundation parents have been selected and inherited. Here, we deep‐sequenced seven historic foundation parents, comprising four cultivars introduced from the former Soviet Union (108Ф, C1470, 611Б and KK1543) and three from United States and Africa (DPL15, STV2B and UGDM), and re‐sequenced sixty‐nine Xinjiang modern cultivars. Phylogenetic analysis of more than 2 million high‐quality single nucleotide polymorphisms allowed their classification two groups, suggesting that Xinjiang Upland cotton cultivars were not only spawned from 108Ф, C1470, 611Б and KK1543, but also had a close kinship with DPL15, STV2B and UGDM. Notably, identity‐by‐descent (IBD) tracking demonstrated that the former Soviet Union cultivars have made a huge contribution to modern cultivar improvement in Xinjiang. A total of 156 selective sweeps were identified. Among them, apoptosis‐antagonizing transcription factor gene (GhAATF1) and mitochondrial transcription termination factor family protein gene (GhmTERF1) were highly involved in the determination of lint percentage. Additionally, the auxin response factor gene (GhARF3) located in inherited IBD segments from 108Ф and 611Б was highly correlated with fibre quality. These results provide an insight into the genomics of artificial selection for improving cotton production and facilitate next‐generation precision breeding of cotton and other crops.

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The cotton (Gossypium hirsutum) pigment gland is a distinctive structure that functions as the main deposit organ of gossypol and its derivatives. It is also an ideal system in which to study cell differentiation and organogenesis. However, only a few genes that determine the process of gland formation have been reported, including GoPGF, CGP1, and CGFs; the molecular mechanisms underlying gland initiation are still largely unclear. Here, we report the discovery of the novel stem pigment gland-forming gene GoSPGF by map-based cloning; annotated as a GRAS transcription factor, this gene is responsible for the glandless trait specifically on the stem. In the stem glandless mutant T582, a point mutation (C to A) was found to create a premature stop codon and truncate the protein. Similarly, virus-induced gene silencing of GoSPGF resulted in glandless stems and dramatically reduced gossypol content. Comparative transcriptomic data showed that loss of GoSPGF significantly suppressed expression of many genes involved in gossypol biosynthesis and altered expression of genes involved in gibberellic acid signaling/biosynthesis. Overall, these findings provide more insight into the networks regulating glandular structure differentiation and formation in cotton, which will be helpful for understanding other plants bearing special gland structures such as tobacco (Nicotiana benthamiana), artemisia annua, mint (Mentha spp.), and rubber (Hevea brasiliensis).

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