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Transcriptome and physiological analysis of class III peroxidase family in ice plant seedlings in response to salt-induced oxidative stress

ABSTRACT: Ice plant (Mesembryanthemum crystallinum L.) is a halophyte and an inducible CAM plant. Ice plant seedlings exhibit moderate salt tolerance, with root growth unaffected by 200 mM NaCl treatments, while hypocotyl elongation is hindered in salt-stressed etiolated seedlings. Superoxide anion accumulation was prominent in cotyledons and primary leaves but decreased in root tissues over time but was not significantly affected by salt treatment. Hydrogen peroxide (H2O2) levels surged initially in both control and salt-treated seedlings, with higher and more persistent H2O2 levels in salt-treated seedlings, indicating salt-induced ROS accumulation, especially in etiolated seedlings. An RNA-seq analysis of etiolated seedlings revealed 6,326 unigenes (about 8%) showing more than a four-fold change in expression after a 6-h 200 mM NaCl treatment. The top GO terms for 4-fold upregulated DEGs in the Molecular Function category included “cation binding,” “metal ion binding,” “oxidoreductase activity,” “monooxygenase activity,” and “antioxidant activity.” The top GO terms for 4-fold down-regulated DEGs in the Biological Process category included “metabolic process”, “cellular metabolic process”, and “biosynthetic process”. Upregulated genes were primarily linked to ion transport and stress responses and downregulated genes to growth processes like ribosomal protein synthesis and cell wall formation. This indicates that salt stress hinders growth but enhances ion homeostasis and stress response mechanisms. For class III peroxidase family genes, 14 out of 53 identified transcripts met the criteria for differentially expressed genes. Quantitative RT-PCR confirmed that the expression of McPrx4.1, McPrx12.1, and McPrx12.3 increased, while the expression of McPrx60.3 decreased. We suggest distinct roles for individual class III peroxidase members in the trade-offs between plant growth and stress response. Unveiling these responses will advance our understanding of the growth–stress balance in the intrinsic salt tolerance in halophytes.

ORGANISM(S): Mesembryanthemum crystallinum

PROVIDER: GSE277109 | GEO | 2025/01/01

REPOSITORIES: GEO

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Project description:Background: The halophyte Mesembryanthemum crystallinum (ice plant) is a model for studying salt tolerance. The morphology, physiology, metabolism, and gene expression of ice plant have been studied for over 40 years. Although the complete genome sequence has not been revealed, large-scale analyses of gene expression profiling have drawn an outline of salt tolerance in ice plant. Despite ample information in the transcriptome, miRNA information has not been documented. Results: We examined responses to a sudden increase in salinity in ice plant seedlings. Using a fluorescent dye to detect Na+, we found that ice plant roots respond to an increased flux of Na+ by either secreting or storing Na+ in specialized cells. High-throughput sequencing was used to identify small RNA profiles in three-day-old seedlings treated with or without 200 mM NaCl. Totally 132 conserved miRNAs belonging to 22 families were found. The hairpin precursor of 19 conserved mcr-miRNAs and 12 novel mcr-miRNAs were identified. Target genes are involved in a broad range of biological processes: transcription factors that regulate growth and development, enzymes that catalyze miRNA biogenesis for the most conserved mcr-miRNA, and proteins that are involved in ion homeostasis and drought-stress responses for some novel mcr-miRNAs. After 6 h of salt stress, the expressions of most mcr-miRNAs were down-regulated, whereas the expressions of their corresponding target genes were up-regulated. Analyses of the functions of target genes revealed that cellular processes, including growth and development, metabolism, and ion transport activity were up-regulated in roots under salt stress. Conclusions: Analyses of small RNA profile of ice plant seedlings identified many conserved miRNA families and several novel miRNAs. The expression of ten conserved miRNAs and three novel miRNAs were reciprocally correlated to predicted targets hourly after salt stress. Based on the expression pattern of miRNA and target genes in combination with the observation of Na+ distribution, we suggest that ice plant roots respond effectively to increased salinity by using Na+ as an osmoticum for cell expansion and guard cell opening. Excessive Na+ could either be secreted through root epidermis or stored in specialized leaf epidermal cells. These responses are partially regulated at the miRNA-mediated post-transcriptional level.

Project description:Large-scale gene expression affected by salt stress was analyzed with tomato seedlings (Lycoperson esculentum Mill cv. Money Maker) by a cDNA microarray (Tom1). The significantly differentially expressed genes (5% Benjamini-Hochberg false discovery rate) consisted of 1757 sequences in the analyzed tissues (cotyledons + shoot tip). Genes with over 2 fold difference were selected from the list and further categorized into different function and cellular processes. Tomato homologous genes for the chaperone proteins, antioxidant enzymes (catalase and peroxidase), and ion transporters (Na+-driven multidrug efflux pump, vacuolar ATPase, and others) were induced. The ACC oxidase and ethylene-responsive gene tomato homologs had higher transcript level after salt treatment. Multiple members with different expression patterns were identified for the bZIP, WRKY, and MADS-box transcription regulator. Different genes in the signal transduction pathway, such as the protein kinases (Shaggy kinase, mitogen-activated protein kinase, ethylene receptor neverripe, and others), protein phosphatases, calmodulin, G-protein, and the N- myristoyltransferase, were regulated by salt stress. Most of the protease and the inhibitor homologs were suppressed by salt stress. In addition, different isoforms of cytochrome P450, genes for polyamine biosynthesis (putrescine and proline) and detoxification compounds (glutathione and thioredoxin), several key enzyme genes in the metabolic pathways of carbohydrates, amino acids, and fatty acids, were also affected by salt treatment. This study has provided a set of candidate genes, especially those in the regulatory machinery that can be further investigated to define salt stress in tomato and other plant species. Keywords: treatment response Effect of 75mM NaCl on gene’s expression in tomato seedlings, Lycoperscon esculentum Mill. cv. Money Maker after 17 d of treatment. Each sample represents a pool of same tissue 20 seedlings grown in two flasks. Experiment was done in triplicate.

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Transcriptome and physiological analysis of class III peroxidase family in ice plant seedlings in response to salt-induced oxidative stress

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