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Metabolomics Analysis Provides New Insights Into the Molecular Mechanisms of Parasitic Plant Dodder Elongation in vitro.

ABSTRACT: Dodder (Cuscuta spp.) species are obligate parasitic flowering plants that totally depend on host plants for growth and reproduction and severely suppress hosts' growth. As a rootless and leafless plant, excised dodder shoots exhibit rapid growth and elongation for several days to hunt for new host stems, and parasitization could be reestablished. This is one unique ability of the dodder to facilitate its success in nature. Clearly, excised dodder stems have to recycle stored nutrients to elongate as much as possible. However, the mechanism of stored nutrient recycling in the in vitro dodder shoots is still poorly understood. Here, we found that dodder is a carbohydrate-rich holoparasitic plant. During the in vitro dodder shoot development, starch was dramatically and thoroughly degraded in the dodder shoots. Sucrose derived from starch degradation in the basal stems was transported to the shoot tips, in which EMP and TCA pathways were activated to compensate for carbon demand for the following elongation according to the variations of sugar content related to the crucial gene expression, and the metabolomics analysis. Additionally, antioxidants were significantly accumulated in the shoot tips in contrast to those in the basal stems. The variations of phytohormones (jasmonic acid, indole-3-acetic acid, and abscisic acid) indicated that they played essential roles in this process. All these data suggested that starch and sucrose degradation, EMP and TCA activation, antioxidants, and phytohormones were crucial and associated with the in vitro dodder shoot elongation.

SUBMITTER: Zhang Y

PROVIDER: S-EPMC9251578 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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.

Project description:UnlabelledFoodborne illness-causing enteric bacteria are able to colonize plant surfaces without causing infection. We lack an understanding of how epiphytic persistence of enteric bacteria occurs on plants, possibly as an adaptive transit strategy to maximize chances of reentering herbivorous hosts. We used tomato (Solanum lycopersicum) cultivars that have exhibited differential susceptibilities to Salmonella enterica colonization to investigate the influence of plant surface compounds and exudates on enteric bacterial populations. Tomato fruit, shoot, and root exudates collected at different developmental stages supported growth of S. enterica to various degrees in a cultivar- and plant organ-dependent manner. S. enterica growth in fruit exudates of various cultivars correlated with epiphytic growth data (R(2) = 0.504; P = 0.006), providing evidence that plant surface compounds drive bacterial colonization success. Chemical profiling of tomato surface compounds with gas chromatography-time of flight mass spectrometry (GC-TOF-MS) provided valuable information about the metabolic environment on fruit, shoot, and root surfaces. Hierarchical cluster analysis of the data revealed quantitative differences in phytocompounds among cultivars and changes over a developmental course and by plant organ (P < 0.002). Sugars, sugar alcohols, and organic acids were associated with increased S. enterica growth, while fatty acids, including palmitic and oleic acids, were negatively correlated. We demonstrate that the plant surface metabolite landscape has a significant impact on S. enterica growth and colonization efficiency. This environmental metabolomics approach provides an avenue to understand interactions between human pathogens and plants that could lead to strategies to identify or breed crop cultivars for microbiologically safer produce.ImportanceIn recent years, fresh produce has emerged as a leading food vehicle for enteric pathogens. Salmonella-contaminated tomatoes represent a recurrent human pathogen-plant commodity pair. We demonstrate that Salmonella can utilize tomato surface compounds and exudates for growth. Surface metabolite profiling revealed that the types and amounts of compounds released to the plant surface differ by cultivar, plant developmental stage, and plant organ. Differences in exudate profiles explain some of the variability in Salmonella colonization susceptibility seen among tomato cultivars. Certain medium- and long-chain fatty acids were associated with restricted Salmonella growth, while sugars, sugar alcohols, and organic acids correlated with larger Salmonella populations. These findings uncover the possibility of selecting crop varieties based on characteristics that impair foodborne pathogen growth for enhanced safety of fresh produce.

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Metabolomics Analysis Provides New Insights Into the Molecular Mechanisms of Parasitic Plant Dodder Elongation in vitro.

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