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
Hauptverfasser: Stupnikova, Irina, Benamar, Abdelilah, Tolleter, Dimitri, Grelet, Johann, Borovskii, Genadii, Dorne, Albert-Jean, Macherel, David
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container_issue 1
container_start_page 326
container_title Plant physiology (Bethesda)
container_volume 140
creator Stupnikova, Irina
Benamar, Abdelilah
Tolleter, Dimitri
Grelet, Johann
Borovskii, Genadii
Dorne, Albert-Jean
Macherel, David
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.
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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. 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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 &amp; 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 &amp; 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 ; 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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 &amp; 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. 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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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