Pea Seed Mitochondria Are Endowed with a Remarkable Tolerance to Extreme Physiological Temperatures
Most seeds are anhydrobiotes, relying on an array of protective and repair mechanisms, and seed mitochondria have previously been shown to harbor stress proteins probably involved in desiccation tolerance. Since temperature stress is a major issue for germinating seeds, the temperature response of p...
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Veröffentlicht in: | Plant physiology (Bethesda) 2006, Vol.140 (1), p.326-335 |
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description | Most seeds are anhydrobiotes, relying on an array of protective and repair mechanisms, and seed mitochondria have previously been shown to harbor stress proteins probably involved in desiccation tolerance. Since temperature stress is a major issue for germinating seeds, the temperature response of pea (Pisum sativum) seed mitochondria was examined in comparison with that of mitochondria from etiolated epicotyl, a desiccation-sensitive tissue. The functional analysis illustrated the remarkable temperature tolerance of seed mitochondria in response to both cold and heat stress. The mitochondria maintained a well-coupled respiration between -3.5°C and 40°C, while epicotyl mitochondria were not efficient below 0°C and collapsed above 30°C. Both mitochondria exhibited a similar Arrhenius break temperature at 7°C, although they differed in phospholipid composition. Seed mitochondria had a lower phosphatidylethanolamine-to-phosphatidylcholine ratio, fewer unsaturated fatty acids, and appeared less susceptible to lipid peroxidation. They also accumulated large amounts of heat shock protein HSP22 and late-embryogenesis abundant protein PsLEAm. The combination of membrane composition and stress protein accumulation required for desiccation tolerance is expected to lead to an unusually wide temperature tolerance, contributing to the fitness of germinating seeds in adverse conditions. The unique oxidation of external NADH at low temperatures found with several types of mitochondria may play a central role in maintaining energy homeostasis during cold shock, a situation often encountered by sessile and ectothermic higher plants. |
doi_str_mv | 10.1104/pp.105.073015 |
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Since temperature stress is a major issue for germinating seeds, the temperature response of pea (Pisum sativum) seed mitochondria was examined in comparison with that of mitochondria from etiolated epicotyl, a desiccation-sensitive tissue. The functional analysis illustrated the remarkable temperature tolerance of seed mitochondria in response to both cold and heat stress. The mitochondria maintained a well-coupled respiration between -3.5°C and 40°C, while epicotyl mitochondria were not efficient below 0°C and collapsed above 30°C. Both mitochondria exhibited a similar Arrhenius break temperature at 7°C, although they differed in phospholipid composition. Seed mitochondria had a lower phosphatidylethanolamine-to-phosphatidylcholine ratio, fewer unsaturated fatty acids, and appeared less susceptible to lipid peroxidation. They also accumulated large amounts of heat shock protein HSP22 and late-embryogenesis abundant protein PsLEAm. The combination of membrane composition and stress protein accumulation required for desiccation tolerance is expected to lead to an unusually wide temperature tolerance, contributing to the fitness of germinating seeds in adverse conditions. The unique oxidation of external NADH at low temperatures found with several types of mitochondria may play a central role in maintaining energy homeostasis during cold shock, a situation often encountered by sessile and ectothermic higher plants.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.105.073015</identifier><identifier>PMID: 16377742</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Acclimatization ; cell respiration ; cold stress ; Cold tolerance ; Environmental Stress and Adaptation to Stress ; Epicotyls ; fatty acid composition ; Fatty Acids - analysis ; Genetics ; Germination ; heat shock proteins ; heat stress ; Heat-Shock Proteins - metabolism ; late-embryogenesis abundant protein ; Life Sciences ; lipid composition ; Lipid Peroxidation ; Lipids ; Low temperature ; Mitochondria ; Mitochondria - chemistry ; Mitochondria - physiology ; Models, Biological ; NAD (coenzyme) ; NAD - metabolism ; Oxidation ; Oxidation-Reduction ; oxidative phosphorylation ; Oxidative stress ; Peas ; Phospholipids - analysis ; Pisum sativum ; Pisum sativum - embryology ; Pisum sativum - physiology ; Pisum sativum - ultrastructure ; plant biochemistry ; plant physiology ; plant proteins ; Plant Proteins - metabolism ; Plant Shoots - anatomy & histology ; Plant Shoots - metabolism ; Plant Shoots - physiology ; Plants ; Plants genetics ; Respiration ; seed germination ; seeds ; Seeds - anatomy & histology ; Seeds - metabolism ; Seeds - physiology ; Temperature</subject><ispartof>Plant physiology (Bethesda), 2006, Vol.140 (1), p.326-335</ispartof><rights>Copyright 2006 American Society of Plant Biologists</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Copyright © 2006, American Society of Plant Biologists 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c500t-b3eee3ed2cc44676cf1e6abc9ba9ce21dc223e00079e499b52422bc9e236e2053</citedby><cites>FETCH-LOGICAL-c500t-b3eee3ed2cc44676cf1e6abc9ba9ce21dc223e00079e499b52422bc9e236e2053</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/4282054$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/4282054$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,777,781,800,882,4010,27904,27905,27906,57998,58231</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16377742$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02665983$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Stupnikova, Irina</creatorcontrib><creatorcontrib>Benamar, Abdelilah</creatorcontrib><creatorcontrib>Tolleter, Dimitri</creatorcontrib><creatorcontrib>Grelet, Johann</creatorcontrib><creatorcontrib>Borovskii, Genadii</creatorcontrib><creatorcontrib>Dorne, Albert-Jean</creatorcontrib><creatorcontrib>Macherel, David</creatorcontrib><title>Pea Seed Mitochondria Are Endowed with a Remarkable Tolerance to Extreme Physiological Temperatures</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Most seeds are anhydrobiotes, relying on an array of protective and repair mechanisms, and seed mitochondria have previously been shown to harbor stress proteins probably involved in desiccation tolerance. Since temperature stress is a major issue for germinating seeds, the temperature response of pea (Pisum sativum) seed mitochondria was examined in comparison with that of mitochondria from etiolated epicotyl, a desiccation-sensitive tissue. The functional analysis illustrated the remarkable temperature tolerance of seed mitochondria in response to both cold and heat stress. The mitochondria maintained a well-coupled respiration between -3.5°C and 40°C, while epicotyl mitochondria were not efficient below 0°C and collapsed above 30°C. Both mitochondria exhibited a similar Arrhenius break temperature at 7°C, although they differed in phospholipid composition. Seed mitochondria had a lower phosphatidylethanolamine-to-phosphatidylcholine ratio, fewer unsaturated fatty acids, and appeared less susceptible to lipid peroxidation. They also accumulated large amounts of heat shock protein HSP22 and late-embryogenesis abundant protein PsLEAm. The combination of membrane composition and stress protein accumulation required for desiccation tolerance is expected to lead to an unusually wide temperature tolerance, contributing to the fitness of germinating seeds in adverse conditions. The unique oxidation of external NADH at low temperatures found with several types of mitochondria may play a central role in maintaining energy homeostasis during cold shock, a situation often encountered by sessile and ectothermic higher plants.</description><subject>Acclimatization</subject><subject>cell respiration</subject><subject>cold stress</subject><subject>Cold tolerance</subject><subject>Environmental Stress and Adaptation to Stress</subject><subject>Epicotyls</subject><subject>fatty acid composition</subject><subject>Fatty Acids - analysis</subject><subject>Genetics</subject><subject>Germination</subject><subject>heat shock proteins</subject><subject>heat stress</subject><subject>Heat-Shock Proteins - metabolism</subject><subject>late-embryogenesis abundant protein</subject><subject>Life Sciences</subject><subject>lipid composition</subject><subject>Lipid Peroxidation</subject><subject>Lipids</subject><subject>Low temperature</subject><subject>Mitochondria</subject><subject>Mitochondria - chemistry</subject><subject>Mitochondria - physiology</subject><subject>Models, Biological</subject><subject>NAD (coenzyme)</subject><subject>NAD - metabolism</subject><subject>Oxidation</subject><subject>Oxidation-Reduction</subject><subject>oxidative phosphorylation</subject><subject>Oxidative stress</subject><subject>Peas</subject><subject>Phospholipids - analysis</subject><subject>Pisum sativum</subject><subject>Pisum sativum - embryology</subject><subject>Pisum sativum - physiology</subject><subject>Pisum sativum - ultrastructure</subject><subject>plant biochemistry</subject><subject>plant physiology</subject><subject>plant proteins</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Shoots - anatomy & histology</subject><subject>Plant Shoots - metabolism</subject><subject>Plant Shoots - physiology</subject><subject>Plants</subject><subject>Plants genetics</subject><subject>Respiration</subject><subject>seed germination</subject><subject>seeds</subject><subject>Seeds - anatomy & histology</subject><subject>Seeds - metabolism</subject><subject>Seeds - physiology</subject><subject>Temperature</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUtv1DAUhS0EokNhyQ6BV0gsMlw_4iQbpFE1UKRBVHS6thznzsQliVM709J_j6uMymPlK5_P5_roEPKawZIxkB_HcckgX0IhgOVPyILlgmc8l-VTsgBIM5RldUJexHgNAEww-ZycMCWKopB8QewFGnqJ2NBvbvK29UMTnKGrgHQ9NP4uCXduaqmhP7A34aepO6Rb32Ewg0U6ebr-NQXskV6099H5zu-dNR3dYj8mZjoEjC_Js53pIr46nqfk6vN6e3aebb5_-Xq22mQ2B5iyWiCiwIZbK6UqlN0xVKa2VW0qi5w1lnOBKURRoayqOueS8yQjFwo55OKUfJp9x0PdY2NxmILp9Bhc-vm99sbpf5XBtXrvbzUTXEEuk8GH2aD979n5aqMf7oArlVeluGWJfX9cFvzNAeOkexctdp0Z0B-iLkApIRgkMJtBG3yMAXePzgz0Q4V6HNOY67nCxL_9O8Uf-thZAt7MwHWcfHjUJS_5HOLdLO-M12YfXNRXlzw1D2lXxRUXvwFum6q7</recordid><startdate>2006</startdate><enddate>2006</enddate><creator>Stupnikova, Irina</creator><creator>Benamar, Abdelilah</creator><creator>Tolleter, Dimitri</creator><creator>Grelet, Johann</creator><creator>Borovskii, Genadii</creator><creator>Dorne, Albert-Jean</creator><creator>Macherel, David</creator><general>American Society of Plant Biologists</general><general>Oxford University Press ; American Society of Plant Biologists</general><scope>FBQ</scope><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><scope>1XC</scope><scope>5PM</scope></search><sort><creationdate>2006</creationdate><title>Pea Seed Mitochondria Are Endowed with a Remarkable Tolerance to Extreme Physiological Temperatures</title><author>Stupnikova, Irina ; Benamar, Abdelilah ; Tolleter, Dimitri ; Grelet, Johann ; Borovskii, Genadii ; Dorne, Albert-Jean ; Macherel, David</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c500t-b3eee3ed2cc44676cf1e6abc9ba9ce21dc223e00079e499b52422bc9e236e2053</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>Acclimatization</topic><topic>cell respiration</topic><topic>cold stress</topic><topic>Cold tolerance</topic><topic>Environmental Stress and Adaptation to Stress</topic><topic>Epicotyls</topic><topic>fatty acid composition</topic><topic>Fatty Acids - analysis</topic><topic>Genetics</topic><topic>Germination</topic><topic>heat shock proteins</topic><topic>heat stress</topic><topic>Heat-Shock Proteins - metabolism</topic><topic>late-embryogenesis abundant protein</topic><topic>Life Sciences</topic><topic>lipid composition</topic><topic>Lipid Peroxidation</topic><topic>Lipids</topic><topic>Low temperature</topic><topic>Mitochondria</topic><topic>Mitochondria - chemistry</topic><topic>Mitochondria - physiology</topic><topic>Models, Biological</topic><topic>NAD (coenzyme)</topic><topic>NAD - metabolism</topic><topic>Oxidation</topic><topic>Oxidation-Reduction</topic><topic>oxidative phosphorylation</topic><topic>Oxidative stress</topic><topic>Peas</topic><topic>Phospholipids - analysis</topic><topic>Pisum sativum</topic><topic>Pisum sativum - embryology</topic><topic>Pisum sativum - physiology</topic><topic>Pisum sativum - ultrastructure</topic><topic>plant biochemistry</topic><topic>plant physiology</topic><topic>plant proteins</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Shoots - anatomy & histology</topic><topic>Plant Shoots - metabolism</topic><topic>Plant Shoots - physiology</topic><topic>Plants</topic><topic>Plants genetics</topic><topic>Respiration</topic><topic>seed germination</topic><topic>seeds</topic><topic>Seeds - anatomy & histology</topic><topic>Seeds - metabolism</topic><topic>Seeds - physiology</topic><topic>Temperature</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Stupnikova, Irina</creatorcontrib><creatorcontrib>Benamar, Abdelilah</creatorcontrib><creatorcontrib>Tolleter, Dimitri</creatorcontrib><creatorcontrib>Grelet, Johann</creatorcontrib><creatorcontrib>Borovskii, Genadii</creatorcontrib><creatorcontrib>Dorne, Albert-Jean</creatorcontrib><creatorcontrib>Macherel, David</creatorcontrib><collection>AGRIS</collection><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><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Stupnikova, Irina</au><au>Benamar, Abdelilah</au><au>Tolleter, Dimitri</au><au>Grelet, Johann</au><au>Borovskii, Genadii</au><au>Dorne, Albert-Jean</au><au>Macherel, David</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pea Seed Mitochondria Are Endowed with a Remarkable Tolerance to Extreme Physiological Temperatures</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2006</date><risdate>2006</risdate><volume>140</volume><issue>1</issue><spage>326</spage><epage>335</epage><pages>326-335</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><abstract>Most seeds are anhydrobiotes, relying on an array of protective and repair mechanisms, and seed mitochondria have previously been shown to harbor stress proteins probably involved in desiccation tolerance. Since temperature stress is a major issue for germinating seeds, the temperature response of pea (Pisum sativum) seed mitochondria was examined in comparison with that of mitochondria from etiolated epicotyl, a desiccation-sensitive tissue. The functional analysis illustrated the remarkable temperature tolerance of seed mitochondria in response to both cold and heat stress. The mitochondria maintained a well-coupled respiration between -3.5°C and 40°C, while epicotyl mitochondria were not efficient below 0°C and collapsed above 30°C. Both mitochondria exhibited a similar Arrhenius break temperature at 7°C, although they differed in phospholipid composition. Seed mitochondria had a lower phosphatidylethanolamine-to-phosphatidylcholine ratio, fewer unsaturated fatty acids, and appeared less susceptible to lipid peroxidation. They also accumulated large amounts of heat shock protein HSP22 and late-embryogenesis abundant protein PsLEAm. The combination of membrane composition and stress protein accumulation required for desiccation tolerance is expected to lead to an unusually wide temperature tolerance, contributing to the fitness of germinating seeds in adverse conditions. The unique oxidation of external NADH at low temperatures found with several types of mitochondria may play a central role in maintaining energy homeostasis during cold shock, a situation often encountered by sessile and ectothermic higher plants.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>16377742</pmid><doi>10.1104/pp.105.073015</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Acclimatization cell respiration cold stress Cold tolerance Environmental Stress and Adaptation to Stress Epicotyls fatty acid composition Fatty Acids - analysis Genetics Germination heat shock proteins heat stress Heat-Shock Proteins - metabolism late-embryogenesis abundant protein Life Sciences lipid composition Lipid Peroxidation Lipids Low temperature Mitochondria Mitochondria - chemistry Mitochondria - physiology Models, Biological NAD (coenzyme) NAD - metabolism Oxidation Oxidation-Reduction oxidative phosphorylation Oxidative stress Peas Phospholipids - analysis Pisum sativum Pisum sativum - embryology Pisum sativum - physiology Pisum sativum - ultrastructure plant biochemistry plant physiology plant proteins Plant Proteins - metabolism Plant Shoots - anatomy & histology Plant Shoots - metabolism Plant Shoots - physiology Plants Plants genetics Respiration seed germination seeds Seeds - anatomy & histology Seeds - metabolism Seeds - physiology Temperature |
title | Pea Seed Mitochondria Are Endowed with a Remarkable Tolerance to Extreme Physiological Temperatures |
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