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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 lignin biosynthesis in Gb and Gh fibers. The heat map parameters are explained in the legend of Fig. 6
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Fig8: Expression patterns of genes related to lignin biosynthesis in Gb and Gh fibers. The heat map parameters are explained in the legend of Fig. 6

Mentions: The results show that lignin synthesis in commercial cotton fiber is repressed at the transcriptional level. Consistently, no lignin monomers (p-coumaroyl-, coniferyl-, or sinapyl-alcohols) were found in the fiber metabolome, although monolignols were readily detected even in young tree shoots by similar methods [82] (Additional file 3). Nonetheless, 74 loci homologous to lignification-related structural genes [20, 21] (Additional file 17) were expressed in at least one cotton fiber sample, often at low levels. Transcripts encoding three enzymes needed to convert phenylalanine to p-coumaryl CoA were detected (phenylalanine ammonia lyase, PAL; C4-hydroxylase, C4H; and 4-coumaroyl-CoA-ligase, 4CL, or 4CL-like). However, these enzymes support the synthesis of both lignin monomers and flavanoids [83], which were abundant in the cotton fiber metabolome. The flavonoid branch of the phenylpropanoid pathway is modulated by chalcone synthase (CHS, with 3-5 loci expressed in cotton fiber). Alternatively hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase (HCT) controls flux toward lignin. Gb fiber had stronger expression of more HCT loci as compared to Gh fiber, but both genotypes had low expression of only one HCT locus at 28 DPA during SCW synthesis (Fig. 8). Therefore, flux toward lignin may be limited during cotton fiber SCW synthesis despite the (overall low) expression of down-stream genes on the lignin branch pathway. The expression patterns of lignin-related structural genes are displayed in Fig. 8 including homologues of: C3-hydroxylase (C3H); cinnamoyl-CoA reductase-like (CCRL); cinnamyl alcohol dehydrogenase (CAD or CAD-like); ferulate 5-hydroxylase (F5H); caffeoyl-CoA O-methyltransferase (CCOMT of CCOMT-like); and caffeic acid O-methyltransferase (COMT or COMT-like). These could be related to the presence of minor amounts of lignin-like phenolics in cotton fiber [28, 80, 81].Fig. 8


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 lignin biosynthesis 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

Fig8: Expression patterns of genes related to lignin biosynthesis in Gb and Gh fibers. The heat map parameters are explained in the legend of Fig. 6
Mentions: The results show that lignin synthesis in commercial cotton fiber is repressed at the transcriptional level. Consistently, no lignin monomers (p-coumaroyl-, coniferyl-, or sinapyl-alcohols) were found in the fiber metabolome, although monolignols were readily detected even in young tree shoots by similar methods [82] (Additional file 3). Nonetheless, 74 loci homologous to lignification-related structural genes [20, 21] (Additional file 17) were expressed in at least one cotton fiber sample, often at low levels. Transcripts encoding three enzymes needed to convert phenylalanine to p-coumaryl CoA were detected (phenylalanine ammonia lyase, PAL; C4-hydroxylase, C4H; and 4-coumaroyl-CoA-ligase, 4CL, or 4CL-like). However, these enzymes support the synthesis of both lignin monomers and flavanoids [83], which were abundant in the cotton fiber metabolome. The flavonoid branch of the phenylpropanoid pathway is modulated by chalcone synthase (CHS, with 3-5 loci expressed in cotton fiber). Alternatively hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase (HCT) controls flux toward lignin. Gb fiber had stronger expression of more HCT loci as compared to Gh fiber, but both genotypes had low expression of only one HCT locus at 28 DPA during SCW synthesis (Fig. 8). Therefore, flux toward lignin may be limited during cotton fiber SCW synthesis despite the (overall low) expression of down-stream genes on the lignin branch pathway. The expression patterns of lignin-related structural genes are displayed in Fig. 8 including homologues of: C3-hydroxylase (C3H); cinnamoyl-CoA reductase-like (CCRL); cinnamyl alcohol dehydrogenase (CAD or CAD-like); ferulate 5-hydroxylase (F5H); caffeoyl-CoA O-methyltransferase (CCOMT of CCOMT-like); and caffeic acid O-methyltransferase (COMT or COMT-like). These could be related to the presence of minor amounts of lignin-like phenolics in cotton fiber [28, 80, 81].Fig. 8

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