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Comparative transcriptome analysis of short fiber mutants Ligon-lintless 1 and 2 reveals common mechanisms pertinent to fiber elongation in cotton (Gossypium hirsutum L.).

ABSTRACT: Understanding the molecular processes affecting cotton (Gossypium hirsutum) fiber development is important for developing tools aimed at improving fiber quality. Short fiber cotton mutants Ligon-lintless 1 (Li1) and Ligon-lintless 2 (Li2) are naturally occurring, monogenic mutations residing on different chromosomes. Both mutations cause early cessation in fiber elongation. These two mutants serve as excellent model systems to elucidate molecular mechanisms relevant to fiber length development. Previous studies of these mutants using transcriptome analysis by our laboratory and others had been limited by the fact that very large numbers of genes showed altered expression patterns in the mutants, making a targeted analysis difficult or impossible. In this research, a comparative microarray analysis was conducted using these two short fiber mutants and their near isogenic wild type (WT) grown under both field and greenhouse environments in order to identify key genes or metabolic pathways common to fiber elongation. Analyses of three transcriptome profiles obtained from different growth conditions and mutant types showed that most differentially expressed genes (DEGs) were affected by growth conditions. Under field conditions, short fiber mutants commanded higher expression of genes related to energy production, manifested by the increasing of mitochondrial electron transport activity or responding to reactive oxygen species when compared to the WT. Eighty-eight DEGs were identified to have altered expression patterns common to both short fiber mutants regardless of growth conditions. Enrichment, pathway and expression analyses suggested that these 88 genes were likely involved in fiber elongation without being affected by growth conditions.

SUBMITTER: Gilbert MK

PROVIDER: S-EPMC3991655 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Comparative transcriptome analysis of short fiber mutants Ligon-lintless 1 and 2 reveals common mechanisms pertinent to fiber elongation in cotton (Gossypium hirsutum L.).

Gilbert Matthew K MK Kim Hee Jin HJ Tang Yuhong Y Naoumkina Marina M Fang David D DD

PloS one 20140418 4

Understanding the molecular processes affecting cotton (Gossypium hirsutum) fiber development is important for developing tools aimed at improving fiber quality. Short fiber cotton mutants Ligon-lintless 1 (Li1) and Ligon-lintless 2 (Li2) are naturally occurring, monogenic mutations residing on different chromosomes. Both mutations cause early cessation in fiber elongation. These two mutants serve as excellent model systems to elucidate molecular mechanisms relevant to fiber length development. ...[more]

PMID: 24748059

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Project description:BackgroundCotton fiber length is a key determinant of fiber quality for the textile industry. Understanding the molecular basis of fiber elongation would provide a means for improvement of fiber length. Ligon lintless-1 (Li 1 ) and Ligon lintless-2 (Li 2 ) are monogenic and dominant mutations, that result in an extreme reduction in the length of lint fiber to approximately 6 mm on mature seeds. In a near-isogenic state with wild type (WT) cotton these two short fiber mutants provide an excellent model system to study mechanisms of fiber elongation.ResultsWe used next generation sequencing (RNA-seq) to identify common fiber elongation related genes in developing fibers of Li 1 and Li 2 mutants growing in the field and a greenhouse. We found a large number of differentially expressed genes common to both mutants, including 531 up-regulated genes and 652 down-regulated genes. Major intrinsic proteins or aquaporins were one of the most significantly over-represented gene families among common down-regulated genes in Li 1 and Li 2 fibers. The members of three subfamilies of aquaporins, including plasma membrane intrinsic proteins, tonoplast intrinsic proteins and NOD26-like intrinsic proteins were down-regulated in short fiber mutants. The osmotic concentration and the concentrations of soluble sugars were lower in fiber cells of both short fiber mutants than in WT, whereas the concentrations of K+ and malic acid were significantly higher in mutants during rapid cell elongation.ConclusionsWe found that the aquaporins were the most down-regulated gene family in both short fiber mutants. The osmolality and concentrations of soluble sugars were less in saps of Li 1 - Li 2 , whereas the concentrations of malic acid, K+ and other detected ions were significantly higher in saps of mutants than in WT. These results suggest that higher accumulation of ions in fiber cells, reduced osmotic pressure and low expression of aquaporins, may contribute to the cessation of fiber elongation in Li 1 and Li 2 short-fiber mutants. The research presented here provides new insights into osmoregulation of short fiber mutants and the role of aquaporins in cotton fiber elongation.

Project description:BACKGROUND: Cotton fiber length is very important to the quality of textiles. Understanding the genetics and physiology of cotton fiber elongation can provide valuable tools to the cotton industry by targeting genes or other molecules responsible for fiber elongation. Ligon Lintless-1 (Li1) is a monogenic mutant in Upland cotton (Gossypium hirsutum) which exhibits an early cessation of fiber elongation resulting in very short fibers (< 6 mm) at maturity. This presents an excellent model system for studying the underlying molecular and cellular processes involved with cotton fiber elongation. Previous reports have characterized Li1 at early cell wall elongation and during later secondary cell wall synthesis, however there has been very limited analysis of the transition period between these developmental time points. RESULTS: Physical and morphological measurements of the Li1 mutant fibers were conducted, including measurement of the cellulose content during development. Affymetrix microarrays were used to analyze transcript profiles at the critical developmental time points of 3 days post anthesis (DPA), the late elongation stage of 12 DPA and the early secondary cell wall synthesis stage of 16 DPA. The results indicated severe disruption to key hormonal and other pathways related to fiber development, especially pertaining to the transition stage from elongation to secondary cell wall synthesis. Gene Ontology enrichment analysis identified several key pathways at the transition stage that exhibited altered regulation. Genes involved in ethylene biosynthesis and primary cell wall rearrangement were affected, and a primary cell wall-related cellulose synthase was transcriptionally repressed. Linkage mapping using a population of 2,553 F2 individuals identified SSR markers associated with the Li1 genetic locus on chromosome 22. Linkage mapping in combination with utilizing the diploid G. raimondii genome sequences permitted additional analysis of the region containing the Li1 gene. CONCLUSIONS: The early termination of fiber elongation in the Li1 mutant is likely controlled by an early upstream regulatory factor resulting in the altered regulation of hundreds of downstream genes. Several elongation-related genes that exhibited altered expression profiles in the Li1 mutant were identified. Molecular markers closely associated with the Li1 locus were developed. Results presented here will lay the foundation for further investigation of the genetic and molecular mechanisms of fiber elongation.

Project description:BackgroundThe 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.ResultsPrincipal 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.ConclusionsThis 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.

Project description:BackgroundImproving the yield and fiber quality of upland cotton is a goal of plant breeders. However, increasing the yield and quality of cotton fibers is becoming more urgent. While the growing human population needs more cotton fiber, climate change is reducing the amount of land on which cotton can be planted, or making it difficult to ensure that water and other resources will be available in optimal quantities. The most logical means of improving yield and quality is understanding and manipulating the genes involved. Here, we used comparative transcriptomics to explore differences in gene expression between long- and short-fiber cotton lines to identify candidate genes useful for cotton improvement.ResultsLight and electron microscopy revealed that the initial fiber density was significantly greater in our short-fiber group (SFG) than in our long-fiber group (LFG). Compared with the SFG fibers, the LFG fibers were longer at all developmental stages. Comparison of the LFG and SFG transcriptomes revealed a total of 3538 differentially expressed genes (DEGs). Notably, at all three developmental stages examined, two expression patterns, consistently downregulated (profile 0) and consistently upregulated (profile 7), were identified, and both were significantly enriched in the SFG and LFG. Twenty-two DEGs known to be involved in fiber initiation were detected in profile 0, while 31 DEGs involved in fiber elongation were detected in profile 7. Functional annotation suggested that these DEGs, which included ERF1, TUA2, TUB1, and PER64, affect fiber elongation by participating in the ethylene response, microtubule synthesis, and/or the peroxidase (POD) catalytic pathway. qRT-PCR was used to confirm the RNA sequencing results for select genes.ConclusionsA comparison of SFG and LFG transcription profiles revealed modest but important differences in gene expression between the groups. Notably, our results confirm those of previous studies suggesting that genes involved in ethylene, tubulin, and POD pathways play important roles in fiber development. The 22 consistently downregulated DEGs involved in fiber initiation and the 31 consistently upregulated genes involved in fiber elongation are seemingly good candidate genes for improving fiber initiation and elongation in cotton.

Project description:BackgroundCotton fiber length is an important quality attribute to the textile industry and longer fibers can be more efficiently spun into yarns to produce superior fabrics. There is typically a negative correlation between yield and fiber quality traits such as length. An understanding of the regulatory mechanisms controlling fiber length can potentially provide a valuable tool for cotton breeders to improve fiber length while maintaining high yields. The cotton (Gossypium hirsutum L.) fiber mutation Ligon lintless-2 is controlled by a single dominant gene (Li2) that results in significantly shorter fibers than a wild-type. In a near-isogenic state with a wild-type cotton line, Li2 is a model system with which to study fiber elongation.ResultsTwo near-isogenic lines of Ligon lintless-2 (Li2) cotton, one mutant and one wild-type, were developed through five generations of backcrosses (BC5). An F2 population was developed from a cross between the two Li2 near-isogenic lines and used to develop a linkage map of the Li2 locus on chromosome 18. Five simple sequence repeat (SSR) markers were closely mapped around the Li2 locus region with two of the markers flanking the Li2 locus at 0.87 and 0.52 centimorgan. No apparent differences in fiber initiation and early fiber elongation were observed between the mutant ovules and the wild-type ones. Gene expression profiling using microarrays suggested roles of reactive oxygen species (ROS) homeostasis and cytokinin regulation in the Li2 mutant phenotype. Microarray gene expression data led to successful identification of an EST-SSR marker (NAU3991) that displayed complete linkage to the Li2 locus.ConclusionsIn the field of cotton genomics, we report the first successful conversion of gene expression data into an SSR marker that is associated with a genomic region harboring a gene responsible for a fiber trait. The EST-derived SSR marker NAU3991 displayed complete linkage to the Li2 locus on chromosome 18 and resided in a gene with similarity to a putative plectin-related protein. The complete linkage suggests that this expressed sequence may be the Li2 gene.

Dataset Information

Comparative transcriptome analysis of short fiber mutants Ligon-lintless 1 and 2 reveals common mechanisms pertinent to fiber elongation in cotton (Gossypium hirsutum L.).

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Comparative transcriptome analysis of short fiber mutants Ligon-lintless 1 and 2 reveals common mechanisms pertinent to fiber elongation in cotton (Gossypium hirsutum L.).

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