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Desiccation Tolerance Mechanism in Resurrection Fern-Ally Selaginella tamariscina Revealed by Physiological and Proteomic Analysis
Drought is one of the most severe limitations to plant growth and productivity. Resurrection plants have evolved a unique capability to tolerate desiccation in vegetative tissues. Fern-ally Selaginella tamariscina (Beauv.) is one of the most primitive vascular resurrection plants, which can survive...
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Published in: | Journal of proteome research 2010-12, Vol.9 (12), p.6561-6577 |
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description | Drought is one of the most severe limitations to plant growth and productivity. Resurrection plants have evolved a unique capability to tolerate desiccation in vegetative tissues. Fern-ally Selaginella tamariscina (Beauv.) is one of the most primitive vascular resurrection plants, which can survive a desiccated state and recover when water becomes available. To better understand the mechanism of desiccation tolerance, we have applied physiological and proteomic analysis. Samples of S. tamariscina were water-deprived for up to seven days followed by 12 h of rewatering. Our results showed that endogenous abscisic acid (ABA) increased to regulate dehydration-responsive genes/proteins and physiological processes. In the course of dehydration, the contents of osmolytes represented by soluble sugars and proline were increased to maintain cell structure integrity. The activities of four antioxidant enzymes (superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and glutathione reductase (GR)) also increased. In contrast, both the rate of photosynthesis and the chlorophyll content decreased, and plasma membrane integrity was lost. We identified 138 desiccation-responsive two-dimensional electrophoresis (2-DE) spots, representing 103 unique proteins. Hierarchical clustering analysis revealed that 83% of the proteins were down-regulated upon dehydration. They were mainly involved in photosynthesis, carbohydrate and energy metabolism, stress and defense, protein metabolism, signaling, membrane/transport, cell structure, and cell division. The dynamic expression changes of the desiccation-responsive proteins provide strong evidence that cell structure modification, photosynthesis reduction, antioxidant system activation, and protein post-transcriptional/translational modifications are essential to the poikilochlorophyllous fern-ally S. tamariscina in response to dehydration. In addition, our comparative analysis of dehydration-responsive proteins in vegetative tissues from 19 desiccation tolerant and nontolerant plant species suggests that resurrection S. tamariscina has developed a specific desiccation tolerant mechanism. To our knowledge, this study constitutes the first detailed investigation of the protein complement in fern/fern-allies. |
doi_str_mv | 10.1021/pr100767k |
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Resurrection plants have evolved a unique capability to tolerate desiccation in vegetative tissues. Fern-ally Selaginella tamariscina (Beauv.) is one of the most primitive vascular resurrection plants, which can survive a desiccated state and recover when water becomes available. To better understand the mechanism of desiccation tolerance, we have applied physiological and proteomic analysis. Samples of S. tamariscina were water-deprived for up to seven days followed by 12 h of rewatering. Our results showed that endogenous abscisic acid (ABA) increased to regulate dehydration-responsive genes/proteins and physiological processes. In the course of dehydration, the contents of osmolytes represented by soluble sugars and proline were increased to maintain cell structure integrity. The activities of four antioxidant enzymes (superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and glutathione reductase (GR)) also increased. In contrast, both the rate of photosynthesis and the chlorophyll content decreased, and plasma membrane integrity was lost. We identified 138 desiccation-responsive two-dimensional electrophoresis (2-DE) spots, representing 103 unique proteins. Hierarchical clustering analysis revealed that 83% of the proteins were down-regulated upon dehydration. They were mainly involved in photosynthesis, carbohydrate and energy metabolism, stress and defense, protein metabolism, signaling, membrane/transport, cell structure, and cell division. The dynamic expression changes of the desiccation-responsive proteins provide strong evidence that cell structure modification, photosynthesis reduction, antioxidant system activation, and protein post-transcriptional/translational modifications are essential to the poikilochlorophyllous fern-ally S. tamariscina in response to dehydration. In addition, our comparative analysis of dehydration-responsive proteins in vegetative tissues from 19 desiccation tolerant and nontolerant plant species suggests that resurrection S. tamariscina has developed a specific desiccation tolerant mechanism. To our knowledge, this study constitutes the first detailed investigation of the protein complement in fern/fern-allies.</description><identifier>ISSN: 1535-3893</identifier><identifier>EISSN: 1535-3907</identifier><identifier>DOI: 10.1021/pr100767k</identifier><identifier>PMID: 20923197</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Abscisic Acid - metabolism ; Adaptation, Physiological ; Catalase - metabolism ; Chlorophyll - metabolism ; Electrophoresis, Gel, Two-Dimensional ; Glutathione Reductase - metabolism ; Osmotic Pressure - drug effects ; Peroxidase - metabolism ; Photosynthesis - drug effects ; Plant Proteins - analysis ; Plant Proteins - metabolism ; Proteome - analysis ; Proteome - metabolism ; Proteomics - methods ; Selaginellaceae - drug effects ; Selaginellaceae - metabolism ; Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization ; Stress, Physiological ; Superoxide Dismutase - metabolism ; Time Factors ; Water - metabolism ; Water - pharmacology</subject><ispartof>Journal of proteome research, 2010-12, Vol.9 (12), p.6561-6577</ispartof><rights>Copyright © 2010 American Chemical Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a314t-7ebf5587d6cb2a7cbf0b6e998afb5759a8cc2fdb1855220bdfdc4a8237448b613</citedby><cites>FETCH-LOGICAL-a314t-7ebf5587d6cb2a7cbf0b6e998afb5759a8cc2fdb1855220bdfdc4a8237448b613</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20923197$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Xiaonan</creatorcontrib><creatorcontrib>Chen, Sixue</creatorcontrib><creatorcontrib>Zhang, Heng</creatorcontrib><creatorcontrib>Shi, Lei</creatorcontrib><creatorcontrib>Cao, Fenglin</creatorcontrib><creatorcontrib>Guo, Lihai</creatorcontrib><creatorcontrib>Xie, Yongming</creatorcontrib><creatorcontrib>Wang, Tai</creatorcontrib><creatorcontrib>Yan, Xiufeng</creatorcontrib><creatorcontrib>Dai, Shaojun</creatorcontrib><title>Desiccation Tolerance Mechanism in Resurrection Fern-Ally Selaginella tamariscina Revealed by Physiological and Proteomic Analysis</title><title>Journal of proteome research</title><addtitle>J. Proteome Res</addtitle><description>Drought is one of the most severe limitations to plant growth and productivity. Resurrection plants have evolved a unique capability to tolerate desiccation in vegetative tissues. Fern-ally Selaginella tamariscina (Beauv.) is one of the most primitive vascular resurrection plants, which can survive a desiccated state and recover when water becomes available. To better understand the mechanism of desiccation tolerance, we have applied physiological and proteomic analysis. Samples of S. tamariscina were water-deprived for up to seven days followed by 12 h of rewatering. Our results showed that endogenous abscisic acid (ABA) increased to regulate dehydration-responsive genes/proteins and physiological processes. In the course of dehydration, the contents of osmolytes represented by soluble sugars and proline were increased to maintain cell structure integrity. The activities of four antioxidant enzymes (superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and glutathione reductase (GR)) also increased. In contrast, both the rate of photosynthesis and the chlorophyll content decreased, and plasma membrane integrity was lost. We identified 138 desiccation-responsive two-dimensional electrophoresis (2-DE) spots, representing 103 unique proteins. Hierarchical clustering analysis revealed that 83% of the proteins were down-regulated upon dehydration. They were mainly involved in photosynthesis, carbohydrate and energy metabolism, stress and defense, protein metabolism, signaling, membrane/transport, cell structure, and cell division. The dynamic expression changes of the desiccation-responsive proteins provide strong evidence that cell structure modification, photosynthesis reduction, antioxidant system activation, and protein post-transcriptional/translational modifications are essential to the poikilochlorophyllous fern-ally S. tamariscina in response to dehydration. In addition, our comparative analysis of dehydration-responsive proteins in vegetative tissues from 19 desiccation tolerant and nontolerant plant species suggests that resurrection S. tamariscina has developed a specific desiccation tolerant mechanism. To our knowledge, this study constitutes the first detailed investigation of the protein complement in fern/fern-allies.</description><subject>Abscisic Acid - metabolism</subject><subject>Adaptation, Physiological</subject><subject>Catalase - metabolism</subject><subject>Chlorophyll - metabolism</subject><subject>Electrophoresis, Gel, Two-Dimensional</subject><subject>Glutathione Reductase - metabolism</subject><subject>Osmotic Pressure - drug effects</subject><subject>Peroxidase - metabolism</subject><subject>Photosynthesis - drug effects</subject><subject>Plant Proteins - analysis</subject><subject>Plant Proteins - metabolism</subject><subject>Proteome - analysis</subject><subject>Proteome - metabolism</subject><subject>Proteomics - methods</subject><subject>Selaginellaceae - drug effects</subject><subject>Selaginellaceae - metabolism</subject><subject>Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization</subject><subject>Stress, Physiological</subject><subject>Superoxide Dismutase - metabolism</subject><subject>Time Factors</subject><subject>Water - metabolism</subject><subject>Water - pharmacology</subject><issn>1535-3893</issn><issn>1535-3907</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><recordid>eNpt0E1P3DAQBmALgfhqD_0DlS-o4hCwkzh2jqttlyKBQHR7jsbOBAyOvdhJpb3yywndhRMnj-RHr2ZeQr5xdsZZzs9XkTMmK_m0Qw65KERW1Ezuvs-qLg7IUUqPjHEhWbFPDnJW5wWv5SF5-YnJGgODDZ4ug8MI3iC9RvMA3qaeWk_vMI0xovlvFhh9NnNuTf-gg3vr0TmgA_QQbTLWw8T_IThsqV7T24d1ssGFe2vAUfAtvY1hwNBbQ2ce3PSbvpC9DlzCr9v3mPxd_FrOf2dXNxeX89lVBgUvh0yi7oRQsq2MzkEa3TFdYV0r6LSQogZlTN61mish8pzptmtNCSovZFkqXfHimPzY5K5ieB4xDU0_bfy2vscwpkZxVZUVF2qSpxtpYkgpYtesop0OXDecNW-NNx-NT_b7NnXUPbYf8r3iCZxsAJjUPIYxTmenT4JeAfxhisM</recordid><startdate>20101203</startdate><enddate>20101203</enddate><creator>Wang, Xiaonan</creator><creator>Chen, Sixue</creator><creator>Zhang, Heng</creator><creator>Shi, Lei</creator><creator>Cao, Fenglin</creator><creator>Guo, Lihai</creator><creator>Xie, Yongming</creator><creator>Wang, Tai</creator><creator>Yan, Xiufeng</creator><creator>Dai, Shaojun</creator><general>American Chemical Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20101203</creationdate><title>Desiccation Tolerance Mechanism in Resurrection Fern-Ally Selaginella tamariscina Revealed by Physiological and Proteomic Analysis</title><author>Wang, Xiaonan ; Chen, Sixue ; Zhang, Heng ; Shi, Lei ; Cao, Fenglin ; Guo, Lihai ; Xie, Yongming ; Wang, Tai ; Yan, Xiufeng ; Dai, Shaojun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a314t-7ebf5587d6cb2a7cbf0b6e998afb5759a8cc2fdb1855220bdfdc4a8237448b613</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Abscisic Acid - metabolism</topic><topic>Adaptation, Physiological</topic><topic>Catalase - metabolism</topic><topic>Chlorophyll - metabolism</topic><topic>Electrophoresis, Gel, Two-Dimensional</topic><topic>Glutathione Reductase - metabolism</topic><topic>Osmotic Pressure - drug effects</topic><topic>Peroxidase - metabolism</topic><topic>Photosynthesis - drug effects</topic><topic>Plant Proteins - analysis</topic><topic>Plant Proteins - metabolism</topic><topic>Proteome - analysis</topic><topic>Proteome - metabolism</topic><topic>Proteomics - methods</topic><topic>Selaginellaceae - drug effects</topic><topic>Selaginellaceae - metabolism</topic><topic>Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization</topic><topic>Stress, Physiological</topic><topic>Superoxide Dismutase - metabolism</topic><topic>Time Factors</topic><topic>Water - metabolism</topic><topic>Water - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Xiaonan</creatorcontrib><creatorcontrib>Chen, Sixue</creatorcontrib><creatorcontrib>Zhang, Heng</creatorcontrib><creatorcontrib>Shi, Lei</creatorcontrib><creatorcontrib>Cao, Fenglin</creatorcontrib><creatorcontrib>Guo, Lihai</creatorcontrib><creatorcontrib>Xie, Yongming</creatorcontrib><creatorcontrib>Wang, Tai</creatorcontrib><creatorcontrib>Yan, Xiufeng</creatorcontrib><creatorcontrib>Dai, Shaojun</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of proteome research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Xiaonan</au><au>Chen, Sixue</au><au>Zhang, Heng</au><au>Shi, Lei</au><au>Cao, Fenglin</au><au>Guo, Lihai</au><au>Xie, Yongming</au><au>Wang, Tai</au><au>Yan, Xiufeng</au><au>Dai, Shaojun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Desiccation Tolerance Mechanism in Resurrection Fern-Ally Selaginella tamariscina Revealed by Physiological and Proteomic Analysis</atitle><jtitle>Journal of proteome research</jtitle><addtitle>J. Proteome Res</addtitle><date>2010-12-03</date><risdate>2010</risdate><volume>9</volume><issue>12</issue><spage>6561</spage><epage>6577</epage><pages>6561-6577</pages><issn>1535-3893</issn><eissn>1535-3907</eissn><abstract>Drought is one of the most severe limitations to plant growth and productivity. Resurrection plants have evolved a unique capability to tolerate desiccation in vegetative tissues. Fern-ally Selaginella tamariscina (Beauv.) is one of the most primitive vascular resurrection plants, which can survive a desiccated state and recover when water becomes available. To better understand the mechanism of desiccation tolerance, we have applied physiological and proteomic analysis. Samples of S. tamariscina were water-deprived for up to seven days followed by 12 h of rewatering. Our results showed that endogenous abscisic acid (ABA) increased to regulate dehydration-responsive genes/proteins and physiological processes. In the course of dehydration, the contents of osmolytes represented by soluble sugars and proline were increased to maintain cell structure integrity. The activities of four antioxidant enzymes (superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and glutathione reductase (GR)) also increased. In contrast, both the rate of photosynthesis and the chlorophyll content decreased, and plasma membrane integrity was lost. We identified 138 desiccation-responsive two-dimensional electrophoresis (2-DE) spots, representing 103 unique proteins. Hierarchical clustering analysis revealed that 83% of the proteins were down-regulated upon dehydration. They were mainly involved in photosynthesis, carbohydrate and energy metabolism, stress and defense, protein metabolism, signaling, membrane/transport, cell structure, and cell division. The dynamic expression changes of the desiccation-responsive proteins provide strong evidence that cell structure modification, photosynthesis reduction, antioxidant system activation, and protein post-transcriptional/translational modifications are essential to the poikilochlorophyllous fern-ally S. tamariscina in response to dehydration. In addition, our comparative analysis of dehydration-responsive proteins in vegetative tissues from 19 desiccation tolerant and nontolerant plant species suggests that resurrection S. tamariscina has developed a specific desiccation tolerant mechanism. To our knowledge, this study constitutes the first detailed investigation of the protein complement in fern/fern-allies.</abstract><cop>United States</cop><pub>American Chemical Society</pub><pmid>20923197</pmid><doi>10.1021/pr100767k</doi><tpages>17</tpages></addata></record> |
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subjects | Abscisic Acid - metabolism Adaptation, Physiological Catalase - metabolism Chlorophyll - metabolism Electrophoresis, Gel, Two-Dimensional Glutathione Reductase - metabolism Osmotic Pressure - drug effects Peroxidase - metabolism Photosynthesis - drug effects Plant Proteins - analysis Plant Proteins - metabolism Proteome - analysis Proteome - metabolism Proteomics - methods Selaginellaceae - drug effects Selaginellaceae - metabolism Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization Stress, Physiological Superoxide Dismutase - metabolism Time Factors Water - metabolism Water - pharmacology |
title | Desiccation Tolerance Mechanism in Resurrection Fern-Ally Selaginella tamariscina Revealed by Physiological and Proteomic Analysis |
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