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

Tuttle JR, Nah G, Duke MV, Alexander DC, Guan X, Song Q, Chen ZJ, Scheffler BE, Haigler CH - BMC Genomics (2015)

Bottom Line: Oxidative stress was lower in the fiber of G. barbadense cv Phytogen 800 as compared to G. hirsutum cv Deltapine 90.Correspondingly, the G. barbadense cultivar had enhanced capacity for management of reactive oxygen species during its prolonged elongation period, as indicated by a 138-fold increase in ascorbate concentration at 28 DPA.The data showed how lignification can be transcriptionally repressed during secondary cell wall synthesis, and they implicated enhanced capacity to manage reactive oxygen species through the ascorbate-glutathione cycle as a positive contributor to fiber length.

View Article: PubMed Central - PubMed

Affiliation: Department of Crop Science, North Carolina State University, Raleigh, NC, 27695, USA. jrtuttle@ncsu.edu.

ABSTRACT

Background: The morphogenesis of single-celled cotton fiber includes extreme elongation and staged cell wall differentiation. Designing strategies for improving cotton fiber for textiles and other uses relies on uncovering the related regulatory mechanisms. In this research we compared the transcriptomes and metabolomes of two Gossypium genotypes, Gossypium barbadense cv Phytogen 800 and G. hirsutum cv Deltapine 90. When grown in parallel, the two types of fiber developed similarly except for prolonged fiber elongation in the G. barbadense cultivar. The data were collected from isolated fibers between 10 to 28 days post anthesis (DPA) representing: primary wall synthesis to support elongation; transitional cell wall remodeling; and secondary wall cellulose synthesis, which was accompanied by continuing elongation only in G. barbadense fiber.

Results: Of 206 identified fiber metabolites, 205 were held in common between the two genotypes. Approximately 38,000 transcripts were expressed in the fiber of each genotype, 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 genotypes with several novel implications. Transitional cell wall remodeling is a distinct stable developmental stage lasting at least four days (18 to 21 DPA). Expression of selected cell wall related transcripts was similar between genotypes, but cellulose synthase gene expression patterns were more complex than expected. Lignification was transcriptionally repressed in both genotypes. Oxidative stress was lower in the fiber of G. barbadense cv Phytogen 800 as compared to G. hirsutum cv Deltapine 90. Correspondingly, the G. barbadense cultivar had enhanced capacity for management of reactive oxygen species during its prolonged elongation period, as indicated by a 138-fold increase in ascorbate concentration at 28 DPA.

Conclusions: The parallel data on deep-sequencing transcriptomics and non-targeted metabolomics for two genotypes of single-celled cotton fiber showed that a discrete developmental stage of transitional cell wall remodeling occurs before secondary wall cellulose synthesis begins. The data showed how lignification can be transcriptionally repressed during secondary cell wall synthesis, and they implicated enhanced capacity to manage reactive oxygen species through the ascorbate-glutathione cycle as a positive contributor to fiber length.

No MeSH data available.


Related in: MedlinePlus

Quantitative changes in the transcriptome and metabolome within and between Gb and Gh fibers. Upper panel: the numbers of transcripts with at least 2 fold up- or downregulation (q ≤ 0.001). Lower panel: the numbers of metabolites with different concentrations (p ≤ 0.05). Each panel shows data for Gb fiber (top, white) and Gh fiber (bottom, black). On the horizontal axis, numbers are placed nearest the DPA when that number of transcripts or metabolites was higher. On the vertical axis, italicized numbers are placed nearest the genotype in which the transcripts or metabolites were higher on each DPA. The comparisons at 10 vs 28 DPA are also shown to highlight the contrast between primary and secondary wall synthesis, a comparison that is most distinct for Gh fiber that is no longer elongating at 28 DPA
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Fig1: Quantitative changes in the transcriptome and metabolome within and between Gb and Gh fibers. Upper panel: the numbers of transcripts with at least 2 fold up- or downregulation (q ≤ 0.001). Lower panel: the numbers of metabolites with different concentrations (p ≤ 0.05). Each panel shows data for Gb fiber (top, white) and Gh fiber (bottom, black). On the horizontal axis, numbers are placed nearest the DPA when that number of transcripts or metabolites was higher. On the vertical axis, italicized numbers are placed nearest the genotype in which the transcripts or metabolites were higher on each DPA. The comparisons at 10 vs 28 DPA are also shown to highlight the contrast between primary and secondary wall synthesis, a comparison that is most distinct for Gh fiber that is no longer elongating at 28 DPA

Mentions: We analyzed the changes in transcripts across the time-course of fiber development within one genotype and at the same DPA across genotypes (Fig. 1). Notably, about 88 % of the transcripts were expressed at 10 DPA in Gh or Gb fiber (33,310 or 33,837 transcripts, respectively), with similar expression levels maintained through 21 DPA. Some of these are alternative transcripts from the same locus, and the 10 DPA unique transcripts are homologous to 14,006 or 14,344 (37–38 %) of the 37,505 protein-coding loci in Gr D-genome diploid cotton. The largest change in gene expression for the fiber of both genotypes occurred between 21 to 28 DPA, representing the shift to predominantly SCW cellulose synthesis. By reference to 21 DPA, more transcripts were downregulated at 28 DPA (11,395 or 11,588 for Gh or Gb) than were upregulated (2971 or 3335 for Gh or Gb). This resulted in 23,834 or 24,297 transcripts expressed in 28 DPA Gb or Gh fiber (Additional files 1 and 2). Comparing 10 and 28 DPA, representing the dominance of primary vs secondary wall synthesis, similarly showed 15,074–15,881 downregulated transcripts at 28 DPA as compared to 4,125–4,149 upregulated transcripts. The GO terms that were overrepresented by the transcripts of both genotypes at 28 DPA compared to 21 DPA include: SCW biogenesis, cellulose microfibril organization, and numerous carbohydrate terms (sucrose, fructose, xylose, mannose, galactose, starch, trehalose). In addition, the overrepresented GO terms reflected the regulation of a major developmental shift: activation of MAPKK activity, negative regulation of ethylene-mediated signaling pathway, and transmembrane receptor protein serine/threonine kinase signaling pathway (Table 2). The homologous Gr gene IDs in each GO category can be found in Additional file 8.Fig. 1


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

Tuttle JR, Nah G, Duke MV, Alexander DC, Guan X, Song Q, Chen ZJ, Scheffler BE, Haigler CH - BMC Genomics (2015)

Quantitative changes in the transcriptome and metabolome within and between Gb and Gh fibers. Upper panel: the numbers of transcripts with at least 2 fold up- or downregulation (q ≤ 0.001). Lower panel: the numbers of metabolites with different concentrations (p ≤ 0.05). Each panel shows data for Gb fiber (top, white) and Gh fiber (bottom, black). On the horizontal axis, numbers are placed nearest the DPA when that number of transcripts or metabolites was higher. On the vertical axis, italicized numbers are placed nearest the genotype in which the transcripts or metabolites were higher on each DPA. The comparisons at 10 vs 28 DPA are also shown to highlight the contrast between primary and secondary wall synthesis, a comparison that is most distinct for Gh fiber that is no longer elongating at 28 DPA
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4482290&req=5

Fig1: Quantitative changes in the transcriptome and metabolome within and between Gb and Gh fibers. Upper panel: the numbers of transcripts with at least 2 fold up- or downregulation (q ≤ 0.001). Lower panel: the numbers of metabolites with different concentrations (p ≤ 0.05). Each panel shows data for Gb fiber (top, white) and Gh fiber (bottom, black). On the horizontal axis, numbers are placed nearest the DPA when that number of transcripts or metabolites was higher. On the vertical axis, italicized numbers are placed nearest the genotype in which the transcripts or metabolites were higher on each DPA. The comparisons at 10 vs 28 DPA are also shown to highlight the contrast between primary and secondary wall synthesis, a comparison that is most distinct for Gh fiber that is no longer elongating at 28 DPA
Mentions: We analyzed the changes in transcripts across the time-course of fiber development within one genotype and at the same DPA across genotypes (Fig. 1). Notably, about 88 % of the transcripts were expressed at 10 DPA in Gh or Gb fiber (33,310 or 33,837 transcripts, respectively), with similar expression levels maintained through 21 DPA. Some of these are alternative transcripts from the same locus, and the 10 DPA unique transcripts are homologous to 14,006 or 14,344 (37–38 %) of the 37,505 protein-coding loci in Gr D-genome diploid cotton. The largest change in gene expression for the fiber of both genotypes occurred between 21 to 28 DPA, representing the shift to predominantly SCW cellulose synthesis. By reference to 21 DPA, more transcripts were downregulated at 28 DPA (11,395 or 11,588 for Gh or Gb) than were upregulated (2971 or 3335 for Gh or Gb). This resulted in 23,834 or 24,297 transcripts expressed in 28 DPA Gb or Gh fiber (Additional files 1 and 2). Comparing 10 and 28 DPA, representing the dominance of primary vs secondary wall synthesis, similarly showed 15,074–15,881 downregulated transcripts at 28 DPA as compared to 4,125–4,149 upregulated transcripts. The GO terms that were overrepresented by the transcripts of both genotypes at 28 DPA compared to 21 DPA include: SCW biogenesis, cellulose microfibril organization, and numerous carbohydrate terms (sucrose, fructose, xylose, mannose, galactose, starch, trehalose). In addition, the overrepresented GO terms reflected the regulation of a major developmental shift: activation of MAPKK activity, negative regulation of ethylene-mediated signaling pathway, and transmembrane receptor protein serine/threonine kinase signaling pathway (Table 2). The homologous Gr gene IDs in each GO category can be found in Additional file 8.Fig. 1

Bottom Line: Oxidative stress was lower in the fiber of G. barbadense cv Phytogen 800 as compared to G. hirsutum cv Deltapine 90.Correspondingly, the G. barbadense cultivar had enhanced capacity for management of reactive oxygen species during its prolonged elongation period, as indicated by a 138-fold increase in ascorbate concentration at 28 DPA.The data showed how lignification can be transcriptionally repressed during secondary cell wall synthesis, and they implicated enhanced capacity to manage reactive oxygen species through the ascorbate-glutathione cycle as a positive contributor to fiber length.

View Article: PubMed Central - PubMed

Affiliation: Department of Crop Science, North Carolina State University, Raleigh, NC, 27695, USA. jrtuttle@ncsu.edu.

ABSTRACT

Background: The morphogenesis of single-celled cotton fiber includes extreme elongation and staged cell wall differentiation. Designing strategies for improving cotton fiber for textiles and other uses relies on uncovering the related regulatory mechanisms. In this research we compared the transcriptomes and metabolomes of two Gossypium genotypes, Gossypium barbadense cv Phytogen 800 and G. hirsutum cv Deltapine 90. When grown in parallel, the two types of fiber developed similarly except for prolonged fiber elongation in the G. barbadense cultivar. The data were collected from isolated fibers between 10 to 28 days post anthesis (DPA) representing: primary wall synthesis to support elongation; transitional cell wall remodeling; and secondary wall cellulose synthesis, which was accompanied by continuing elongation only in G. barbadense fiber.

Results: Of 206 identified fiber metabolites, 205 were held in common between the two genotypes. Approximately 38,000 transcripts were expressed in the fiber of each genotype, 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 genotypes with several novel implications. Transitional cell wall remodeling is a distinct stable developmental stage lasting at least four days (18 to 21 DPA). Expression of selected cell wall related transcripts was similar between genotypes, but cellulose synthase gene expression patterns were more complex than expected. Lignification was transcriptionally repressed in both genotypes. Oxidative stress was lower in the fiber of G. barbadense cv Phytogen 800 as compared to G. hirsutum cv Deltapine 90. Correspondingly, the G. barbadense cultivar had enhanced capacity for management of reactive oxygen species during its prolonged elongation period, as indicated by a 138-fold increase in ascorbate concentration at 28 DPA.

Conclusions: The parallel data on deep-sequencing transcriptomics and non-targeted metabolomics for two genotypes of single-celled cotton fiber showed that a discrete developmental stage of transitional cell wall remodeling occurs before secondary wall cellulose synthesis begins. The data showed how lignification can be transcriptionally repressed during secondary cell wall synthesis, and they implicated enhanced capacity to manage reactive oxygen species through the ascorbate-glutathione cycle as a positive contributor to fiber length.

No MeSH data available.


Related in: MedlinePlus