The SWEET (sugars will eventually be exported transporters) proteins are sugar efflux transporters containing the MtN3_saliva domain, which affects plant development as well as responses to biotic and abiotic stresses. These proteins have not been functionally characterized in the tetraploid cotton, Gossypium hirsutum, which is a widely cultivated cotton species. In this study, we comprehensively analyzed the cotton SWEET gene family. A total of 55 putative G. hirsutum SWEET genes were identified. The GhSWEET genes were classified into four clades based on a phylogenetic analysis and on the examination of gene structural features. Moreover, chromosomal localization and an analysis of homologous genes in Gossypium arboreum, Gossypium raimondii, and G. hirsutum suggested that a whole-genome duplication, several tandem duplications, and a polyploidy event contributed to the expansion of the cotton SWEET gene family, especially in Clade III and IV. Analyses of cis-acting regulatory elements in the promoter regions, expression profiles, and artificial selection revealed that the GhSWEET genes were likely involved in cotton developmental processes and responses to diverse stresses. These findings may clarify the evolution of G. hirsutum SWEET gene family and may provide a foundation for future functional studies of SWEET proteins regarding cotton development and responses to abiotic stresses.

Summary: Upland cotton (Gossypium hirsutum) is the world's largest source of natural fibre and dominates the global textile industry. Hybrid cotton varieties exhibit strong heterosis that confers high fibre yields, yet the genome‐wide effects of artificial selection that have influenced Upland cotton during its breeding history are poorly understood. Here, we resequenced Upland cotton genomes and constructed a variation map of an intact breeding pedigree comprising seven elite and 19 backbone parents. Compared to wild accessions, the 26 pedigree accessions underwent strong artificial selection during domestication that has resulted in reduced genetic diversity but stronger linkage disequilibrium and higher extents of selective sweeps. In contrast to the backbone parents, the elite parents have acquired significantly improved agronomic traits, with an especially pronounced increase in the lint percentage. Notably, identify by descent (IBD) tracking revealed that the elite parents inherited abundant beneficial trait segments and loci from the backbone parents and our combined analyses led to the identification of a core genomic segment which was inherited in the elite lines from the parents Zhong 7263 and Ejing 1 and that was strongly associated with lint percentage. Additionally, SNP correlation analysis of this core segment showed that a non‐synonymous SNP (A‐to‐G) site in a gene encoding the cell wall‐associated receptor‐like kinase 3 (GhWAKL3) protein was highly correlated with increased lint percentage. Our results substantially increase the valuable genomics resources available for future genetic and functional genomics studies of cotton and reveal insights that will facilitate yield increases in the molecular breeding of cotton.

In plants, glucose (Glc) plays important roles, as a nutrient and signal molecule, in the regulation of growth and development. However, the function of Glc in fiber development of upland cotton (Gossypium hirsutum) is unclear. Here, using gas chromatography-mass spectrometry (GC-MS), we found that the Glc content in fibers was higher than that in ovules during the fiber elongation stage. In vitro ovule culture revealed that lower Glc concentrations promoted cotton fiber elongation, while higher concentrations had inhibitory effects. The hexokinase inhibitor N-acetylglucosamine (NAG) inhibited cotton fiber elongation in the cultured ovules, indicating that Glc-mediated fiber elongation depends on the Glc signal transduced by hexokinase. RNA sequencing (RNA-seq) analysis and hormone content detection showed that 150mM Glc significantly activated brassinosteroid (BR) biosynthesis, and the expression of signaling-related genes was also increased, which promoted fiber elongation. In vitro ovule culture clarified that BR induced cotton fiber elongation in a dose-dependent manner. In hormone recovery experiments, only BR compensated for the inhibitory effects of NAG on fiber elongation in a Glc-containing medium. However, the ovules cultured with the BR biosynthetic inhibitor brassinazole and from the BR-deficient cotton mutant pag1 had greatly reduced fiber elongation at all the Glc concentrations tested. This demonstrates that Glc does not compensate for the inhibition of fiber elongation caused by BR biosynthetic defects, suggesting that the BR signaling pathway works downstream of Glc during cotton fiber elongation. Altogether, our study showed that Glc plays an important role in cotton fibre elongation, and crosstalk occurs between Glc and BR signaling during modulation of fiber elongation.