Functional divergence of cellulose synthase orthologs in between wild Gossypium raimondii and domesticated G. arboreum diploid cotton species

Abstract

Cellulose synthase (CESA) synthesizes cellulose for plant cell walls and determines plant morphology and biomass amount. The recently sequenced cotton genomes of two diploid species, Gossypium raimondii and G. arboreum have become references for study of agriculturally important cotton fibers composed nearly exclusively of cellulose. To better understand the roles of functionally divergent CESAs, we compared physical properties and CESA expression patterns from various tissues at different developmental stages of the two diploid cottons. Chemical and phenotypic analyses showed that the domesticated G. arboreum fibers with high cellulose content, thick cell wall, and long length were superior to the wild G. raimondii fibers. Among the seventeen orthologous CESA pairs sharing > 98% identity between the two diploid genomes, putatively nonfunctional CESAs lacking structural integrity or conserved catalytic motifs were identified. Transcript expression patterns of functional CESA family genes sharing high sequence similarities in each genome were determined by RNA-seq and a PCR method that distinguished specific CESAs based on single nucleotide polymorphisms. Our results showed that mutational events causing non-functionalization and tissue specific expression patterns of the redundant CESA genes occurred in the domesticated G. arboreum more frequently than the wild G. raimondii. The results provide insight on how cellulose biosynthesis has been altered during diploid cotton evolution and domestication process, and contributed to the diversity of cotton species that differ in fiber quality and cellulose content.

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Acknowledgments

This research was supported by the USDA-ARS Research Project # 6054-21000-017-00D, and Cotton Incorporated-sponsored project #19-858. Authors thank Dr. Marina Naoumkina of USDA-ARS, Southern Regional Research Center, and Dr. Maojun Wang of Huazhong Agricultural University for their inputs and feedbacks on the manuscript. Authors acknowledge Ms. Tracy Condon for fiber sample preparation, Ms. Holly King for microscopic images, and Mr. Wilson Buttram and Keith Stevenson for preparing cotton fields. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U. S. Department of Agriculture which is an equal opportunity provider and employer.

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Kim, H.J., Thyssen, G.N., Song, X. et al. Functional divergence of cellulose synthase orthologs in between wild Gossypium raimondii and domesticated G. arboreum diploid cotton species. Cellulose 26, 9483–9501 (2019). https://doi.org/10.1007/s10570-019-02744-y

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Keywords

  • Cellulose synthase (CESA)
  • Cotton fiber
  • Gene expression
  • Non-functionalization
  • Sub-functionalization