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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

Expression patterns of genes related to ROS management via the glutathione-ascorbate cycle and the glutathione-perioxidase cycle in Gb and Gh fibers. The heat map parameters are explained in the legend of Fig. 6
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Fig9: Expression patterns of genes related to ROS management via the glutathione-ascorbate cycle and the glutathione-perioxidase cycle in Gb and Gh fibers. The heat map parameters are explained in the legend of Fig. 6

Mentions: The heat map of expression levels of genes related to ROS management via the glutathione-ascorbate cycle [84] is shown in Fig. 9, and the combined transcriptomic and metabolomics data are shown in Fig. 10. The relevant specialized cotton fiber metabolites that were detected in this study included gulono-1,4-lactone, ascorbate, dehydroascorbate, nicotinamide adenine dinucleotide (NAD+), and reduced and oxidized glutathione (GSH and GSSG). Relevant cotton fiber transcripts were homologous to genes encoding gulono-1,4-lactone oxidase (GLOase, or GulLO6), APX, monodehydroascorbate reductase (MDHAR or MDAR), DHAR, glutathione disulfide-reductase (GSR, or GR), and glutathione-dependent peroxidase (GPX) (Additional file 17). At neutral pH most ascorbate is in the form of ascorbate(H−), a reducing agent/anti-oxidant that readily donates a hydrogen atom/electron to H2O2, converting it to harmless H2O in a reaction modulated by APX. The (often short-lived) monodehydroascorbate product can donate a second electron to yield dehydroascorbate in a non-enzymatic process. Reduced ascorbate can be regenerated by: (a) MDHAR using monodehydroascorbate and NADH cofactor; or (b) DHAR using dehydroascorbate and reduced glutathione cofactor. In addition, reduced glutathione acts as an anti-oxidant through donating an electron to H2O2 or oxidized biomolecules, followed by formation of dimeric oxidized glutathione, as catalyzed by GPX enzyme activity. A low GSH:GSSG ratio has been used as a metabolic indicator of oxidative stress in plants [85], and GSR enzyme activity maintains the pool of GSH that is available for ROS scavenging and use as a co-factor during replenishment of the ascorbate pool via DHAR activity.Fig. 9


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)

Expression patterns of genes related to ROS management via the glutathione-ascorbate cycle and the glutathione-perioxidase cycle in Gb and Gh fibers. The heat map parameters are explained in the legend of Fig. 6
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig9: Expression patterns of genes related to ROS management via the glutathione-ascorbate cycle and the glutathione-perioxidase cycle in Gb and Gh fibers. The heat map parameters are explained in the legend of Fig. 6
Mentions: The heat map of expression levels of genes related to ROS management via the glutathione-ascorbate cycle [84] is shown in Fig. 9, and the combined transcriptomic and metabolomics data are shown in Fig. 10. The relevant specialized cotton fiber metabolites that were detected in this study included gulono-1,4-lactone, ascorbate, dehydroascorbate, nicotinamide adenine dinucleotide (NAD+), and reduced and oxidized glutathione (GSH and GSSG). Relevant cotton fiber transcripts were homologous to genes encoding gulono-1,4-lactone oxidase (GLOase, or GulLO6), APX, monodehydroascorbate reductase (MDHAR or MDAR), DHAR, glutathione disulfide-reductase (GSR, or GR), and glutathione-dependent peroxidase (GPX) (Additional file 17). At neutral pH most ascorbate is in the form of ascorbate(H−), a reducing agent/anti-oxidant that readily donates a hydrogen atom/electron to H2O2, converting it to harmless H2O in a reaction modulated by APX. The (often short-lived) monodehydroascorbate product can donate a second electron to yield dehydroascorbate in a non-enzymatic process. Reduced ascorbate can be regenerated by: (a) MDHAR using monodehydroascorbate and NADH cofactor; or (b) DHAR using dehydroascorbate and reduced glutathione cofactor. In addition, reduced glutathione acts as an anti-oxidant through donating an electron to H2O2 or oxidized biomolecules, followed by formation of dimeric oxidized glutathione, as catalyzed by GPX enzyme activity. A low GSH:GSSG ratio has been used as a metabolic indicator of oxidative stress in plants [85], and GSR enzyme activity maintains the pool of GSH that is available for ROS scavenging and use as a co-factor during replenishment of the ascorbate pool via DHAR activity.Fig. 9

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