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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.


Total protein content in 10 to 28 DPA Gh and Gb fiber. Total protein was determined by Bradford assay and normalized to the dry weight of Gb (grey bars) and Gh (white bars) fiber. Mean values ± SD derive from 5 biological replicates at each DPA. Asterisks indicate a significant difference (p ≤ 0.017) between genotypes at each DPA as determined by t-test
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Fig4: Total protein content in 10 to 28 DPA Gh and Gb fiber. Total protein was determined by Bradford assay and normalized to the dry weight of Gb (grey bars) and Gh (white bars) fiber. Mean values ± SD derive from 5 biological replicates at each DPA. Asterisks indicate a significant difference (p ≤ 0.017) between genotypes at each DPA as determined by t-test

Mentions: On each DPA, Gh fiber had 53–78 metabolites with higher concentration than Gb fiber, whereas Gb fiber had 21–47 higher concentration metabolites as compared to Gh fiber (Fig. 1). There were 23–33 dipeptides that were more highly concentrated on each DPA in Gh fiber, with only glycyltryptophan having higher concentration in Gb fiber (Additional file 3). The list of metabolites with greatest concentration difference (≥8-fold) in Gh as compared to Gb fiber showed 12 of 25 cases occurring at 10 DPA, with the list dominated by dipeptides (Table 4). Here, the ≥8-fold threshold was chosen to focus the discussion, and one metabolite is sometimes listed on multiple DPA. More dipeptides in Gh fiber contrasted with higher total protein content in Gb fibers throughout fiber development (Fig. 4). Overall the data support more active protein turnover in Gh fiber. The list of metabolites with ≥8-fold difference in Gb as compared to Gh fiber was dominated (13 of 20 cases) by antioxidants (including flavonoids, glutathione and ascorbate) at diverse DPA, although 7 of 20 cases occur at 28 DPA (Table 4). The section on ROS management contains additional related discussion.Table 4


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)

Total protein content in 10 to 28 DPA Gh and Gb fiber. Total protein was determined by Bradford assay and normalized to the dry weight of Gb (grey bars) and Gh (white bars) fiber. Mean values ± SD derive from 5 biological replicates at each DPA. Asterisks indicate a significant difference (p ≤ 0.017) between genotypes at each DPA as determined by t-test
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig4: Total protein content in 10 to 28 DPA Gh and Gb fiber. Total protein was determined by Bradford assay and normalized to the dry weight of Gb (grey bars) and Gh (white bars) fiber. Mean values ± SD derive from 5 biological replicates at each DPA. Asterisks indicate a significant difference (p ≤ 0.017) between genotypes at each DPA as determined by t-test
Mentions: On each DPA, Gh fiber had 53–78 metabolites with higher concentration than Gb fiber, whereas Gb fiber had 21–47 higher concentration metabolites as compared to Gh fiber (Fig. 1). There were 23–33 dipeptides that were more highly concentrated on each DPA in Gh fiber, with only glycyltryptophan having higher concentration in Gb fiber (Additional file 3). The list of metabolites with greatest concentration difference (≥8-fold) in Gh as compared to Gb fiber showed 12 of 25 cases occurring at 10 DPA, with the list dominated by dipeptides (Table 4). Here, the ≥8-fold threshold was chosen to focus the discussion, and one metabolite is sometimes listed on multiple DPA. More dipeptides in Gh fiber contrasted with higher total protein content in Gb fibers throughout fiber development (Fig. 4). Overall the data support more active protein turnover in Gh fiber. The list of metabolites with ≥8-fold difference in Gb as compared to Gh fiber was dominated (13 of 20 cases) by antioxidants (including flavonoids, glutathione and ascorbate) at diverse DPA, although 7 of 20 cases occur at 28 DPA (Table 4). The section on ROS management contains additional related discussion.Table 4

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.