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Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma

The effects of short-term cold stress and long-term cold acclimation on the light reactions of photosynthesis were examined in vivo to assess their contributions to photosynthetic acclimation to low temperature in Arabidopsis thaliana (L.) Heynh.. All photosynthetic measurements were made at the tem...

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Published in:Planta 2001-12, Vol.214 (2), p.295-303
Main Authors: Savitch, Leonid V., Barker-Åstrom, Johan, Ivanov, Alexander G., Hurry, Vaughan, Öquist, Gunnar, Huner, Norman P.A., Gardeström, Per
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Barker-Åstrom, Johan
Ivanov, Alexander G.
Hurry, Vaughan
Öquist, Gunnar
Huner, Norman P.A.
Gardeström, Per
description The effects of short-term cold stress and long-term cold acclimation on the light reactions of photosynthesis were examined in vivo to assess their contributions to photosynthetic acclimation to low temperature in Arabidopsis thaliana (L.) Heynh.. All photosynthetic measurements were made at the temperature of exposure: 23 °C for non-acclimated plants and 5 °C for cold-stressed and cold-acclimated plants. Three-day cold-stress treatments at 5 °C inhibited light-saturated rates of CO2 assimilation and O2 evolution by approximately 75%. The 3-day exposure to 5 °C also increased the proportion of reduced QA by 50%, decreased the yield of PSII electron transport by 65% and decreased PSI activity by 31%. In contrast, long-term cold acclimation resulted in a strong but incomplete recovery of light-saturated photosynthesis at 5 °C. The rates of light-saturated CO2 and O2 gas exchange and the in vivo yield of PSII activity under light-saturating conditions were only 35—40% lower, and the relative redox state of QA only 20% lower, at 5 °C after cold acclimation than in controls at 23 °C. PSI activity showed full recovery during long-term cold acclimation. Neither short-term cold stress nor long-term cold acclimation of Arabidopsis was associated with a limitation in ATP, and both treatments resulted in an increase in the ATP/NADPH ratio. This increase in ATP/NADPH was associated with an inhibition of PSI cyclic electron transport but there was no apparent change in the Mehler reaction activity in either cold-stressed or cold-acclimated leaves. Cold acclimation also resulted in an increase in the reduction state of the stroma, as indicated by an increased total activity and activation state of NADP-dependent malate dehydrogenase, and increased light-dependent activities of the major regulatory enzymes of the oxidative pentosephosphate pathway. We suggest that the photosynthetic capacity during cold stress as well as cold acclimation is altered by limitations at the level of consumption of reducing power in carbon metabolism.
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Heynh.. All photosynthetic measurements were made at the temperature of exposure: 23 °C for non-acclimated plants and 5 °C for cold-stressed and cold-acclimated plants. Three-day cold-stress treatments at 5 °C inhibited light-saturated rates of CO2 assimilation and O2 evolution by approximately 75%. The 3-day exposure to 5 °C also increased the proportion of reduced QA by 50%, decreased the yield of PSII electron transport by 65% and decreased PSI activity by 31%. In contrast, long-term cold acclimation resulted in a strong but incomplete recovery of light-saturated photosynthesis at 5 °C. The rates of light-saturated CO2 and O2 gas exchange and the in vivo yield of PSII activity under light-saturating conditions were only 35—40% lower, and the relative redox state of QA only 20% lower, at 5 °C after cold acclimation than in controls at 23 °C. PSI activity showed full recovery during long-term cold acclimation. Neither short-term cold stress nor long-term cold acclimation of Arabidopsis was associated with a limitation in ATP, and both treatments resulted in an increase in the ATP/NADPH ratio. This increase in ATP/NADPH was associated with an inhibition of PSI cyclic electron transport but there was no apparent change in the Mehler reaction activity in either cold-stressed or cold-acclimated leaves. Cold acclimation also resulted in an increase in the reduction state of the stroma, as indicated by an increased total activity and activation state of NADP-dependent malate dehydrogenase, and increased light-dependent activities of the major regulatory enzymes of the oxidative pentosephosphate pathway. We suggest that the photosynthetic capacity during cold stress as well as cold acclimation is altered by limitations at the level of consumption of reducing power in carbon metabolism.</description><identifier>ISSN: 0032-0935</identifier><identifier>ISSN: 1432-2048</identifier><identifier>EISSN: 1432-2048</identifier><identifier>DOI: 10.1007/s004250100622</identifier><identifier>PMID: 11800395</identifier><identifier>CODEN: PLANAB</identifier><language>eng</language><publisher>Berlin: Springer-Verlag</publisher><subject>Acclimatization ; Acclimatization - physiology ; Adenosine Triphosphate - metabolism ; Animal and plant ecology ; Animal, plant and microbial ecology ; Arabidopsis (cold stress) ; Arabidopsis - physiology ; Autoecology ; Biological and medical sciences ; Calvin cycle ; Carbon - metabolism ; Carbon Dioxide - metabolism ; Carbon Dioxide - radiation effects ; Chlorophyll - metabolism ; Chloroplasts ; Chloroplasts - physiology ; cold acclimation ; Cold Temperature ; Enzymes ; Fluorescence ; Fundamental and applied biological sciences. Psychology ; Irradiance ; Leaves ; Light ; Light-Harvesting Protein Complexes ; Low temperature ; Metabolism ; NAD - metabolism ; NADP - metabolism ; Oxidation-Reduction ; Oxygen Consumption - physiology ; Oxygen Consumption - radiation effects ; Photosynthesis ; Photosynthesis - physiology ; Photosynthesis - radiation effects ; Photosynthesis, respiration. Anabolism, catabolism ; Photosynthetic Reaction Center Complex Proteins - metabolism ; Photosynthetic Reaction Center Complex Proteins - radiation effects ; photosystem I (II) ; Plant Leaves - physiology ; Plant physiology and development ; Plants ; Plants and fungi ; reduction state of stroma ; Starch - metabolism ; Starches ; Sucrose - metabolism</subject><ispartof>Planta, 2001-12, Vol.214 (2), p.295-303</ispartof><rights>Springer-Verlag 2001</rights><rights>2002 INIST-CNRS</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c378t-aeeff386bb7faa255c385b6037298d8e624b59b4429cd2961c2c963ac631a47a3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/23386532$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/23386532$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=13443788$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/11800395$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-44654$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Savitch, Leonid V.</creatorcontrib><creatorcontrib>Barker-Åstrom, Johan</creatorcontrib><creatorcontrib>Ivanov, Alexander G.</creatorcontrib><creatorcontrib>Hurry, Vaughan</creatorcontrib><creatorcontrib>Öquist, Gunnar</creatorcontrib><creatorcontrib>Huner, Norman P.A.</creatorcontrib><creatorcontrib>Gardeström, Per</creatorcontrib><title>Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma</title><title>Planta</title><addtitle>Planta</addtitle><description>The effects of short-term cold stress and long-term cold acclimation on the light reactions of photosynthesis were examined in vivo to assess their contributions to photosynthetic acclimation to low temperature in Arabidopsis thaliana (L.) Heynh.. All photosynthetic measurements were made at the temperature of exposure: 23 °C for non-acclimated plants and 5 °C for cold-stressed and cold-acclimated plants. Three-day cold-stress treatments at 5 °C inhibited light-saturated rates of CO2 assimilation and O2 evolution by approximately 75%. The 3-day exposure to 5 °C also increased the proportion of reduced QA by 50%, decreased the yield of PSII electron transport by 65% and decreased PSI activity by 31%. In contrast, long-term cold acclimation resulted in a strong but incomplete recovery of light-saturated photosynthesis at 5 °C. The rates of light-saturated CO2 and O2 gas exchange and the in vivo yield of PSII activity under light-saturating conditions were only 35—40% lower, and the relative redox state of QA only 20% lower, at 5 °C after cold acclimation than in controls at 23 °C. PSI activity showed full recovery during long-term cold acclimation. 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Psychology</subject><subject>Irradiance</subject><subject>Leaves</subject><subject>Light</subject><subject>Light-Harvesting Protein Complexes</subject><subject>Low temperature</subject><subject>Metabolism</subject><subject>NAD - metabolism</subject><subject>NADP - metabolism</subject><subject>Oxidation-Reduction</subject><subject>Oxygen Consumption - physiology</subject><subject>Oxygen Consumption - radiation effects</subject><subject>Photosynthesis</subject><subject>Photosynthesis - physiology</subject><subject>Photosynthesis - radiation effects</subject><subject>Photosynthesis, respiration. Anabolism, catabolism</subject><subject>Photosynthetic Reaction Center Complex Proteins - metabolism</subject><subject>Photosynthetic Reaction Center Complex Proteins - radiation effects</subject><subject>photosystem I (II)</subject><subject>Plant Leaves - physiology</subject><subject>Plant physiology and development</subject><subject>Plants</subject><subject>Plants and fungi</subject><subject>reduction state of stroma</subject><subject>Starch - metabolism</subject><subject>Starches</subject><subject>Sucrose - metabolism</subject><issn>0032-0935</issn><issn>1432-2048</issn><issn>1432-2048</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2001</creationdate><recordtype>article</recordtype><recordid>eNpVkU2LFDEQhoMo7rh69KjkoqcdTSfpr-MwfsKCF_UaqqvTdpZ0p02lXeb_-EPNOOMuQiBFvU-9BfUy9rwQbwoh6rckhJalyHUl5QO2KbSSWyl085BthMi1aFV5wZ4Q3QiRxbp-zC6KoslaW27Y733wPQdE7yZILsw8DHwXoXN9WMgRTyN4BzPwaGn1ibib88MwLd4mm7sYftl4OI4tY0iBDnMabXLIERZAlw5XHIgCOki257cujRz-WkQLlDvR9iv-25xHOY4-xLB4oMQpxTDBU_ZoAE_22fm_ZN8-vP-6_7S9_vLx8353vUVVN2kL1g6DaqquqwcAWZaomrKrhKpl2_SNraTuyrbTWrbYy7YqUGJbKcBKFaBrUJfs6uRLt3ZZO7PEfJR4MAGceee-70yIP8w6rUbrqtQZf33Clxh-rpaSmRyh9R5mG1YytdTHk7cZ3J5AjIEo2uHOuRDmmKL5L8XMvzwbr91k-3v6HFsGXp0BIAQ_RJjR0T2ndA66aTL34sTdUArxTpcqX6lUUv0BPiyyeA</recordid><startdate>20011201</startdate><enddate>20011201</enddate><creator>Savitch, Leonid V.</creator><creator>Barker-Åstrom, Johan</creator><creator>Ivanov, Alexander G.</creator><creator>Hurry, Vaughan</creator><creator>Öquist, Gunnar</creator><creator>Huner, Norman P.A.</creator><creator>Gardeström, Per</creator><general>Springer-Verlag</general><general>Springer</general><scope>IQODW</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>ADTPV</scope><scope>AOWAS</scope><scope>D93</scope></search><sort><creationdate>20011201</creationdate><title>Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma</title><author>Savitch, Leonid V. ; Barker-Åstrom, Johan ; Ivanov, Alexander G. ; Hurry, Vaughan ; Öquist, Gunnar ; Huner, Norman P.A. ; Gardeström, Per</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c378t-aeeff386bb7faa255c385b6037298d8e624b59b4429cd2961c2c963ac631a47a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2001</creationdate><topic>Acclimatization</topic><topic>Acclimatization - physiology</topic><topic>Adenosine Triphosphate - metabolism</topic><topic>Animal and plant ecology</topic><topic>Animal, plant and microbial ecology</topic><topic>Arabidopsis (cold stress)</topic><topic>Arabidopsis - physiology</topic><topic>Autoecology</topic><topic>Biological and medical sciences</topic><topic>Calvin cycle</topic><topic>Carbon - metabolism</topic><topic>Carbon Dioxide - metabolism</topic><topic>Carbon Dioxide - radiation effects</topic><topic>Chlorophyll - metabolism</topic><topic>Chloroplasts</topic><topic>Chloroplasts - physiology</topic><topic>cold acclimation</topic><topic>Cold Temperature</topic><topic>Enzymes</topic><topic>Fluorescence</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Irradiance</topic><topic>Leaves</topic><topic>Light</topic><topic>Light-Harvesting Protein Complexes</topic><topic>Low temperature</topic><topic>Metabolism</topic><topic>NAD - metabolism</topic><topic>NADP - metabolism</topic><topic>Oxidation-Reduction</topic><topic>Oxygen Consumption - physiology</topic><topic>Oxygen Consumption - radiation effects</topic><topic>Photosynthesis</topic><topic>Photosynthesis - physiology</topic><topic>Photosynthesis - radiation effects</topic><topic>Photosynthesis, respiration. 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Heynh.. All photosynthetic measurements were made at the temperature of exposure: 23 °C for non-acclimated plants and 5 °C for cold-stressed and cold-acclimated plants. Three-day cold-stress treatments at 5 °C inhibited light-saturated rates of CO2 assimilation and O2 evolution by approximately 75%. The 3-day exposure to 5 °C also increased the proportion of reduced QA by 50%, decreased the yield of PSII electron transport by 65% and decreased PSI activity by 31%. In contrast, long-term cold acclimation resulted in a strong but incomplete recovery of light-saturated photosynthesis at 5 °C. The rates of light-saturated CO2 and O2 gas exchange and the in vivo yield of PSII activity under light-saturating conditions were only 35—40% lower, and the relative redox state of QA only 20% lower, at 5 °C after cold acclimation than in controls at 23 °C. PSI activity showed full recovery during long-term cold acclimation. Neither short-term cold stress nor long-term cold acclimation of Arabidopsis was associated with a limitation in ATP, and both treatments resulted in an increase in the ATP/NADPH ratio. This increase in ATP/NADPH was associated with an inhibition of PSI cyclic electron transport but there was no apparent change in the Mehler reaction activity in either cold-stressed or cold-acclimated leaves. Cold acclimation also resulted in an increase in the reduction state of the stroma, as indicated by an increased total activity and activation state of NADP-dependent malate dehydrogenase, and increased light-dependent activities of the major regulatory enzymes of the oxidative pentosephosphate pathway. We suggest that the photosynthetic capacity during cold stress as well as cold acclimation is altered by limitations at the level of consumption of reducing power in carbon metabolism.</abstract><cop>Berlin</cop><pub>Springer-Verlag</pub><pmid>11800395</pmid><doi>10.1007/s004250100622</doi><tpages>9</tpages></addata></record>
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subjects Acclimatization
Acclimatization - physiology
Adenosine Triphosphate - metabolism
Animal and plant ecology
Animal, plant and microbial ecology
Arabidopsis (cold stress)
Arabidopsis - physiology
Autoecology
Biological and medical sciences
Calvin cycle
Carbon - metabolism
Carbon Dioxide - metabolism
Carbon Dioxide - radiation effects
Chlorophyll - metabolism
Chloroplasts
Chloroplasts - physiology
cold acclimation
Cold Temperature
Enzymes
Fluorescence
Fundamental and applied biological sciences. Psychology
Irradiance
Leaves
Light
Light-Harvesting Protein Complexes
Low temperature
Metabolism
NAD - metabolism
NADP - metabolism
Oxidation-Reduction
Oxygen Consumption - physiology
Oxygen Consumption - radiation effects
Photosynthesis
Photosynthesis - physiology
Photosynthesis - radiation effects
Photosynthesis, respiration. Anabolism, catabolism
Photosynthetic Reaction Center Complex Proteins - metabolism
Photosynthetic Reaction Center Complex Proteins - radiation effects
photosystem I (II)
Plant Leaves - physiology
Plant physiology and development
Plants
Plants and fungi
reduction state of stroma
Starch - metabolism
Starches
Sucrose - metabolism
title Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma
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