Comparative multi "omics" profiling of Gossypium hirsutum and Gossypium barbadense fibers at high temporal resolution reveals key differences in polysaccharide composition and associated glycosyltransferases

Sivakumar Swaminathan¹Youngwoo Lee²Corrinne E Grover³Megan F DeTemple³Alither S Mugisha³Lauren E Sichterman³Pengcheng Yang²Jun Xie²Jonathan F Wendel³Daniel B Szymanski²Olga A Zabotina^3*

• ¹Iowa State University, Ames, United States
• ²Purdue University, West Lafayette, United States
• ³Iowa State University of Science and Technology, Ames, United States

Among the two allopolyploid cultivated species of cotton, Gossypium barbadense is known for its superior quality fiber compared to Gossypium hirsutum. Length and strength are key determinants of the fiber quality. Although mature fibers are composed of dried cell walls that mainly consist of cellulose, the dynamic remodeling of pectin, xyloglucan, and xylan polysaccharides during fiber growth significantly impacts the final fiber quality. Comprehensive knowledge of polysaccharides and their biosynthesis during fiber development in cultivated species is crucial for improving fiber quality. In this study, comparative large-scale glycome, transcriptome and proteome profiling were conducted daily on fibers of both cotton species, covering critical stages of fiber development spanning primary cell wall synthesis and the transition to secondary cell wall synthesis. Interspecific comparisons revealed that a delayed deposition of cellulose content, as well as the occurrence of lower levels and differential compositions of non-fucosylated/fucosylated xyloglucans, homogalacturonans, and highly branched rhamnogalacturonan-I polysaccharides, possibly contribute to longer elongation time and longer fiber phenotypes of G. barbadense relative to G. hirsutum. Our study also suggests that differential temporal compositions of arabinoxylans and glucuronoxylans might contribute to the variation in cellulose microfibril arrangement and the strength of fiber that exists between the two species of cotton. Comparative transcriptomic analysis identified differentially accumulated polysaccharide-synthesizing glycosyltransferases that may underlie differences in fiber quality between the two species. Transcripts encoding many cell wall-localized expansins were found to be more abundant in G. barbadense than in G. hirsutum, which could be a contributing factor for the longer fibers of G. barbadense. Overall, these findings expand our understanding of the molecular factors that contribute to fiber quality and provide insights for targeted cotton fiber improvement.