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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.


Metabolomic and transcriptomic evidence that transition-stage Gh fiber experiences more oxidative stress than Gb fiber. a) The ratio of reduced glutathione (GSH) to oxidized glutathione (GSSG) in Gb (grey bars) and Gh (white bars) fiber. The ratio is based on the scaled imputed mean for both metabolites. b) The expression level (RPKM) of a putative alternative oxidase (AOX) gene in Gh (white bars) and Gb (grey bars) fiber as derived from RNA-Seq data. The homologous protein in Arabidopsis (AOX2, At5G64210) attenuates ROS production during respiration [91], and the related Gr transcript is Gorai.005G220500.1. Asterisks indicate significant differences between genotypes at a given DPA. Error bars are standard deviation
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Fig11: Metabolomic and transcriptomic evidence that transition-stage Gh fiber experiences more oxidative stress than Gb fiber. a) The ratio of reduced glutathione (GSH) to oxidized glutathione (GSSG) in Gb (grey bars) and Gh (white bars) fiber. The ratio is based on the scaled imputed mean for both metabolites. b) The expression level (RPKM) of a putative alternative oxidase (AOX) gene in Gh (white bars) and Gb (grey bars) fiber as derived from RNA-Seq data. The homologous protein in Arabidopsis (AOX2, At5G64210) attenuates ROS production during respiration [91], and the related Gr transcript is Gorai.005G220500.1. Asterisks indicate significant differences between genotypes at a given DPA. Error bars are standard deviation

Mentions: Both genotypes showed generally similar GPX transcript levels, but two of three GSR transcripts were higher in Gh fiber. This difference may partly account for the 1.4–2.8-fold higher levels of oxidized glutathione in Gb from 10 to 21 DPA. Reduced glutathione was 4.5–12.6-fold higher in Gb at 18 and 21 DPA during transitional cell wall remodeling, and the GSH:GSSG ratio was higher in Gb fiber (Fig. 11a). Given that a high GSH:GSSG ratio indicates less oxidative stress in plant cells [85], this result is consistent with lower oxidative stress in Gb fiber as compared to Gh fiber. Gb fiber also had significantly lower levels of alternative oxidase transcript (related to Gorai.005G220500.1 and At5g64210/AOX2) at 15 and 18 DPA (with the same trend observed at 21 DPA) (Fig. 11b). AOX is induced during stress to attenuate ROS accumulation and energy production by bypassing the electron transport chain [91], and higher AOX levels are correlated with low fiber quality in the im cotton fiber mutant [92]. Higher oxidative stress in the fiber of Gh cv Deltapine 90 may be one explanation for its lower quality as compared to the fiber of Gb cv Phytogen 800.Fig. 11


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)

Metabolomic and transcriptomic evidence that transition-stage Gh fiber experiences more oxidative stress than Gb fiber. a) The ratio of reduced glutathione (GSH) to oxidized glutathione (GSSG) in Gb (grey bars) and Gh (white bars) fiber. The ratio is based on the scaled imputed mean for both metabolites. b) The expression level (RPKM) of a putative alternative oxidase (AOX) gene in Gh (white bars) and Gb (grey bars) fiber as derived from RNA-Seq data. The homologous protein in Arabidopsis (AOX2, At5G64210) attenuates ROS production during respiration [91], and the related Gr transcript is Gorai.005G220500.1. Asterisks indicate significant differences between genotypes at a given DPA. Error bars are standard deviation
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig11: Metabolomic and transcriptomic evidence that transition-stage Gh fiber experiences more oxidative stress than Gb fiber. a) The ratio of reduced glutathione (GSH) to oxidized glutathione (GSSG) in Gb (grey bars) and Gh (white bars) fiber. The ratio is based on the scaled imputed mean for both metabolites. b) The expression level (RPKM) of a putative alternative oxidase (AOX) gene in Gh (white bars) and Gb (grey bars) fiber as derived from RNA-Seq data. The homologous protein in Arabidopsis (AOX2, At5G64210) attenuates ROS production during respiration [91], and the related Gr transcript is Gorai.005G220500.1. Asterisks indicate significant differences between genotypes at a given DPA. Error bars are standard deviation
Mentions: Both genotypes showed generally similar GPX transcript levels, but two of three GSR transcripts were higher in Gh fiber. This difference may partly account for the 1.4–2.8-fold higher levels of oxidized glutathione in Gb from 10 to 21 DPA. Reduced glutathione was 4.5–12.6-fold higher in Gb at 18 and 21 DPA during transitional cell wall remodeling, and the GSH:GSSG ratio was higher in Gb fiber (Fig. 11a). Given that a high GSH:GSSG ratio indicates less oxidative stress in plant cells [85], this result is consistent with lower oxidative stress in Gb fiber as compared to Gh fiber. Gb fiber also had significantly lower levels of alternative oxidase transcript (related to Gorai.005G220500.1 and At5g64210/AOX2) at 15 and 18 DPA (with the same trend observed at 21 DPA) (Fig. 11b). AOX is induced during stress to attenuate ROS accumulation and energy production by bypassing the electron transport chain [91], and higher AOX levels are correlated with low fiber quality in the im cotton fiber mutant [92]. Higher oxidative stress in the fiber of Gh cv Deltapine 90 may be one explanation for its lower quality as compared to the fiber of Gb cv Phytogen 800.Fig. 11

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.