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Metabolomic and transcriptomic insights into how cotton fiber transitions to secondary wall sythesis, represses lignification, and prolongs elongation

John R. Tuttle, Gyoungju Nah, Mary V. Duke, Danny C. Alexander, Xueying Guan, Qingxin Song, Z. Jeffrey Chen, Brian E. Scheffler, Candace H. Haigler
BMC genomics 2015 v.16 no.477 pp. -
Gossypium barbadense, Gossypium hirsutum, cell walls, cellulose, cellulose synthase, fiber quality, flowering, gene expression regulation, genes, high-throughput nucleotide sequencing, lignification, lint cotton, metabolites, metabolome, metabolomics, morphogenesis, oxidative stress, reactive oxygen species, sclerenchyma, transcription (genetics), transcription factors, transcriptome, transcriptomics
Cotton fiber morphogenesis reflects extreme elongation and staged cell wall differentiation in an easily isolated single cell. Uncovering the cellular control mechanisms can lead to strategies for producing improved cotton fiber for textiles and other uses. To identify potential controls of the higher quality fiber found in Gossypium barbadense as compared to more commonly grown G. hirsutum cotton, we compared the two fiber transcriptomes (as analyzed through Illumina sequencing) and metabolomes between 10 to 28 days post anthesis (DPA). This period included primary wall synthesis, transitional cell wall remodeling, and nearly pure cellulose synthesis. The data were interpreted in the context of detailed prior knowledge about comparative fiber development under well-controlled greenhouse conditions. Results: The two fiber types had 205 identified metabolites held in common. Approximately 38,000 transcripts were expressed in each fiber type, and these were mapped to the reference set and interpreted by homology to known genes. The developmental changes in the transcriptomes and the metabolomes were compared within and across fibers from the two species with several novel implications. Transitional cell wall remodeling is a distinct stable developmental stage lasting as least four days (18 to 21 DPA). Expression of selected cell wall related transcripts was similar between the two fiber types, but cellulose synthase gene expression patterns were more complex than expected. Cotton fiber secondary wall cellulose synthesis is controlled by transcription factors related to the differentiation of sclerenchyma cells in the plant body, but lignification is repressed at the transcriptional level. Oxidative stress was lower in G. barbadense fiber due to enhanced capacity for management of reactive oxygen species, as represented by its 138-fold increase in ascorbate at 28 DPA when its elongation was continuing. Conclusions: The results show the power of synthesizing transcriptomics by deep sequencing and non-targeted metabolomics for two species of single-celled cotton fiber during three key stages of cell wall synthesis. In particular, the data show how lignification can be repressed at the transcriptional level and implicate the improved capacity to manage reactive oxygen species as a likely avenue for increasing the length of G. hirsutum fiber.