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Comparative proteomic and biochemical analyses reveal different molecular events occurring in the process of fiber initiation between wild-type allotetraploid cotton and its fuzzless-lintless mutant.

ABSTRACT: To explore lint fiber initiation-related proteins in allotetraploid cotton (Gossypium hirsutum L.), a comparative proteomic analysis was performed between wild-type cotton (Xu-142) and its fuzzless-lintless mutant (Xu-142-fl) at five developmental time points for lint fiber initiation from -3 to +3 days post-anthesis (dpa). Using two-dimensional gel electrophoresis (2-DE) combined with mass spectrometry (MS) analyses, 91 differentially accumulated protein (DAP) species that are related to fiber initiation were successfully identified, of which 58 preferentially accumulated in the wild-type and 33 species in the fl mutant. These DAPs are involved in various cellular and metabolic processes, mainly including important energy/carbohydrate metabolism, redox homeostasis, amino acid and fatty acid biosynthesis, protein quality control, cytoskeleton dynamics, and anthocyanidin metabolism. Further physiological and biochemical experiments revealed dynamic changes in the carbohydrate flux and H2O2 levels in the cotton fiber initiation process. Compared with those in the fl mutant, the contents of glucose and fructose in wild-type ovules sharply increased after anthesis with a relatively higher rate of amino acid biosynthesis. The relative sugar starvation and lower rate of amino acid biosynthesis in the fl mutant ovules may impede the carbohydrate/energy supply and cell wall synthesis, which is consistent with the proteomic results. However, the H2O2 burst was only observed in the wild-type ovules on the day of anthesis. Cotton boll injection experiments in combination with electron microscope observation collectively indicated that H2O2 burst, which is negatively regulated by ascorbate peroxidases (APx), plays an important role in the fiber initiation process. Taken together, our study demonstrates a putative network of DAP species related to fiber initiation in cotton ovules and provides a foundation for future studies on the specific functions of these proteins in fiber development.

SUBMITTER: Yao Y

PROVIDER: S-EPMC4336136 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Comparative proteomic and biochemical analyses reveal different molecular events occurring in the process of fiber initiation between wild-type allotetraploid cotton and its fuzzless-lintless mutant.

Yao Yuan Y Zhang Bing B Dong Chun-Juan CJ Du Ying Y Jiang Lin L Liu Jin-Yuan JY

PloS one 20150220 2

To explore lint fiber initiation-related proteins in allotetraploid cotton (Gossypium hirsutum L.), a comparative proteomic analysis was performed between wild-type cotton (Xu-142) and its fuzzless-lintless mutant (Xu-142-fl) at five developmental time points for lint fiber initiation from -3 to +3 days post-anthesis (dpa). Using two-dimensional gel electrophoresis (2-DE) combined with mass spectrometry (MS) analyses, 91 differentially accumulated protein (DAP) species that are related to fiber ...[more]

PMID: 25700002

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Project description:BackgroundFuzzless-lintless cotton mutants are considered to be the ideal material to understand the molecular mechanisms involved in fibre cell development. Although there are few reports on transcriptome and proteome analyses in cotton at fibre initiation and elongation stages, there is no comprehensive comparative transcriptome analysis of fibre-bearing and fuzzless-lintless cotton ovules covering fibre initiation to secondary cell wall (SCW) synthesis stages. In the present study, a comparative transcriptome analysis was carried out using G. hirsutum L. cv. MCU5 wild-type (WT) and it's near isogenic fuzzless-lintless (fl) mutant at fibre initiation (0 dpa/days post anthesis), elongation (5, 10 and 15 dpa) and SCW synthesis (20 dpa) stages.ResultsScanning electron microscopy study revealed the delay in the initiation of fibre cells and lack of any further development after 2 dpa in the fl mutant. Transcriptome analysis showed major down regulation of transcripts (90%) at fibre initiation and early elongation (5 dpa) stages in the fl mutant. Majority of the down regulated transcripts at fibre initiation stage in the fl mutant represent calcium and phytohormone mediated signal transduction pathways, biosynthesis of auxin and ethylene and stress responsive transcription factors (TFs). Further, transcripts involved in carbohydrate and lipid metabolisms, mitochondrial electron transport system (mETS) and cell wall loosening and elongation were highly down-regulated at fibre elongation stage (5-15 dpa) in the fl mutant. In addition, cellulose synthases and sucrose synthase C were down-regulated at SCW biosynthesis stage (15-20 dpa). Interestingly, some of the transcripts (~50%) involved in phytohormone signalling and stress responsive transcription factors that were up-regulated at fibre initiation stage in the WT were found to be up-regulated at much later stage (15 dpa) in fl mutant.ConclusionsComparative transcriptome analysis of WT and its near isogenic fl mutant revealed key genes and pathways involved at various stages of fibre development. Our data implicated the significant role of mitochondria mediated energy metabolism during fibre elongation process. The delayed expression of genes involved in phytohormone signalling and stress responsive TFs in the fl mutant suggests the need for a coordinated expression of regulatory mechanisms in fibre cell initiation and differentiation.

Project description:BACKGROUND: The length of cotton fiber is an important agronomic trait characteristic that directly affects the quality of yarn and fabric. The cotton (Gossypium hirsutum L.) fiber mutation, Ligon lintless-2, is controlled by a single dominant gene (Li(2)) and results in extremely shortened lint fibers on mature seeds with no visible pleiotropic effects on vegetative growth and development. The Li(2) mutant phenotype provides an ideal model system to study fiber elongation. To understand metabolic processes involved in cotton fiber elongation, changes in metabolites and transcripts in the Li(2) mutant fibers were compared to wild-type fibers during development. RESULTS: Principal component analysis of metabolites from GC-MS data separated Li(2) mutant fiber samples from WT fiber samples at the WT elongation stage, indicating that the Li(2) mutation altered the metabolome of the mutant fibers. The observed alterations in the Li(2) metabolome included significant reductions in the levels of detected free sugars, sugar alcohols, sugar acids, and sugar phosphates. Biological processes associated with carbohydrate biosynthesis, cell wall loosening, and cytoskeleton were also down-regulated in Li(2) fibers. Gamma-aminobutyric acid, known as a signaling factor in many organisms, was significantly elevated in mutant fibers. Higher accumulation of 2-ketoglutarate, succinate, and malate suggested higher nitrate assimilation in the Li(2) line. Transcriptional activation of genes involved in nitrogen compound metabolism along with changes in the levels of nitrogen transport amino acids suggested re-direction of carbon flow into nitrogen metabolism in Li(2) mutant fibers. CONCLUSIONS: This report provides the first comprehensive analysis of metabolite and transcript changes in response to the Li(2) mutation in elongating fibers. A number of factors associated with cell elongation found in this study will facilitate further research in understanding metabolic processes of cotton fiber elongation.

Dataset Information

Comparative proteomic and biochemical analyses reveal different molecular events occurring in the process of fiber initiation between wild-type allotetraploid cotton and its fuzzless-lintless mutant.

Publications

Comparative proteomic and biochemical analyses reveal different molecular events occurring in the process of fiber initiation between wild-type allotetraploid cotton and its fuzzless-lintless mutant.

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