PoplarV1, Main, Corpus, bibRecord, 001B92

Populus euphratica APYRASE2 Enhances Cold Tolerance by Modulating Vesicular Trafficking and Extracellular ATP in Arabidopsis Plants.

Identifieur interne : 001B92 ( Main/Corpus ); précédent : 001B91; suivant : 001B93

Populus euphratica APYRASE2 Enhances Cold Tolerance by Modulating Vesicular Trafficking and Extracellular ATP in Arabidopsis Plants.

Auteurs : Shurong Deng ; Jian Sun ; Rui Zhao ; Mingquan Ding ; Yinan Zhang ; Yuanling Sun ; Wei Wang ; Yeqing Tan ; Dandan Liu ; Xujun Ma ; Peichen Hou ; Meijuan Wang ; Cunfu Lu ; Xin Shen ; Shaoliang Chen

Source :

Plant physiology [ 1532-2548 ] ; 2015.

RBID : pubmed:26224801

English descriptors

KwdEn :
- Adaptation, Physiological (drug effects), Adenosine Triphosphatases (antagonists & inhibitors), Adenosine Triphosphate (metabolism), Apyrase (antagonists & inhibitors), Apyrase (metabolism), Arabidopsis (drug effects), Arabidopsis (genetics), Arabidopsis (physiology), Cations, Divalent (pharmacology), Cell Survival (drug effects), Cold Temperature (MeSH), Enzyme Inhibitors (pharmacology), Extracellular Space (chemistry), Hydrolysis (MeSH), Plant Proteins (metabolism), Plant Roots (cytology), Plant Roots (drug effects), Plant Roots (metabolism), Plants, Genetically Modified (MeSH), Populus (enzymology), Protein Transport (drug effects), Recombinant Proteins (metabolism), Stress, Physiological (drug effects), Subcellular Fractions (drug effects), Subcellular Fractions (metabolism), Substrate Specificity (drug effects).
MESH :
- chemical , antagonists & inhibitors : Adenosine Triphosphatases, Apyrase.
- chemistry : Extracellular Space.
- cytology : Plant Roots.
- drug effects : Adaptation, Physiological, Arabidopsis, Cell Survival, Plant Roots, Protein Transport, Stress, Physiological, Subcellular Fractions, Substrate Specificity.
- enzymology : Populus.
- genetics : Arabidopsis.
- chemical , metabolism : Adenosine Triphosphate, Apyrase, Plant Proteins, Plant Roots, Recombinant Proteins, Subcellular Fractions.
- chemical , pharmacology : Cations, Divalent, Enzyme Inhibitors.
- physiology : Arabidopsis.
- Cold Temperature, Hydrolysis, Plants, Genetically Modified.

Abstract

Apyrase and extracellular ATP play crucial roles in mediating plant growth and defense responses. In the cold-tolerant poplar, Populus euphratica, low temperatures up-regulate APYRASE2 (PeAPY2) expression in callus cells. We investigated the biochemical characteristics of PeAPY2 and its role in cold tolerance. We found that PeAPY2 predominantly localized to the plasma membrane, but punctate signals also appeared in the endoplasmic reticulum and Golgi apparatus. PeAPY2 exhibited broad substrate specificity, but it most efficiently hydrolyzed purine nucleotides, particularly ATP. PeAPY2 preferred Mg(2+) as a cofactor, and it was insensitive to various, specific ATPase inhibitors. When PeAPY2 was ectopically expressed in Arabidopsis (Arabidopsis thaliana), cold tolerance was enhanced, based on root growth measurements and survival rates. Moreover, under cold stress, PeAPY2-transgenic plants maintained plasma membrane integrity and showed reduced cold-elicited electrolyte leakage compared with wild-type plants. These responses probably resulted from efficient plasma membrane repair via vesicular trafficking. Indeed, transgenic plants showed accelerated endocytosis and exocytosis during cold stress and recovery. We found that low doses of extracellular ATP accelerated vesicular trafficking, but high extracellular ATP inhibited trafficking and reduced cell viability. Cold stress caused significant increases in root medium extracellular ATP. However, under these conditions, PeAPY2-transgenic lines showed greater control of extracellular ATP levels than wild-type plants. We conclude that Arabidopsis plants that overexpressed PeAPY2 could increase membrane repair by accelerating vesicular trafficking and hydrolyzing extracellular ATP to avoid excessive, cold-elicited ATP accumulation in the root medium and, thus, reduced ATP-induced inhibition of vesicular trafficking.

DOI: 10.1104/pp.15.00581
PubMed: 26224801
PubMed Central: PMC4577398

Links to Exploration step

pubmed:26224801

Le document en format XML

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<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
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<author><name sortKey="Sun, Jian" sort="Sun, Jian" uniqKey="Sun J" first="Jian" last="Sun">Jian Sun</name>
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<author><name sortKey="Zhao, Rui" sort="Zhao, Rui" uniqKey="Zhao R" first="Rui" last="Zhao">Rui Zhao</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
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<author><name sortKey="Ding, Mingquan" sort="Ding, Mingquan" uniqKey="Ding M" first="Mingquan" last="Ding">Mingquan Ding</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
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<author><name sortKey="Zhang, Yinan" sort="Zhang, Yinan" uniqKey="Zhang Y" first="Yinan" last="Zhang">Yinan Zhang</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
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<author><name sortKey="Sun, Yuanling" sort="Sun, Yuanling" uniqKey="Sun Y" first="Yuanling" last="Sun">Yuanling Sun</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Wang, Wei" sort="Wang, Wei" uniqKey="Wang W" first="Wei" last="Wang">Wei Wang</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Tan, Yeqing" sort="Tan, Yeqing" uniqKey="Tan Y" first="Yeqing" last="Tan">Yeqing Tan</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Liu, Dandan" sort="Liu, Dandan" uniqKey="Liu D" first="Dandan" last="Liu">Dandan Liu</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Ma, Xujun" sort="Ma, Xujun" uniqKey="Ma X" first="Xujun" last="Ma">Xujun Ma</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Hou, Peichen" sort="Hou, Peichen" uniqKey="Hou P" first="Peichen" last="Hou">Peichen Hou</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Wang, Meijuan" sort="Wang, Meijuan" uniqKey="Wang M" first="Meijuan" last="Wang">Meijuan Wang</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Lu, Cunfu" sort="Lu, Cunfu" uniqKey="Lu C" first="Cunfu" last="Lu">Cunfu Lu</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Shen, Xin" sort="Shen, Xin" uniqKey="Shen X" first="Xin" last="Shen">Xin Shen</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Chen, Shaoliang" sort="Chen, Shaoliang" uniqKey="Chen S" first="Shaoliang" last="Chen">Shaoliang Chen</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.) lschen@bjfu.edu.cn.</nlm:affiliation>
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<idno type="pmc">PMC4577398</idno>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">Populus euphratica APYRASE2 Enhances Cold Tolerance by Modulating Vesicular Trafficking and Extracellular ATP in Arabidopsis Plants.</title>
<author><name sortKey="Deng, Shurong" sort="Deng, Shurong" uniqKey="Deng S" first="Shurong" last="Deng">Shurong Deng</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Sun, Jian" sort="Sun, Jian" uniqKey="Sun J" first="Jian" last="Sun">Jian Sun</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Zhao, Rui" sort="Zhao, Rui" uniqKey="Zhao R" first="Rui" last="Zhao">Rui Zhao</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Ding, Mingquan" sort="Ding, Mingquan" uniqKey="Ding M" first="Mingquan" last="Ding">Mingquan Ding</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Zhang, Yinan" sort="Zhang, Yinan" uniqKey="Zhang Y" first="Yinan" last="Zhang">Yinan Zhang</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Sun, Yuanling" sort="Sun, Yuanling" uniqKey="Sun Y" first="Yuanling" last="Sun">Yuanling Sun</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Wang, Wei" sort="Wang, Wei" uniqKey="Wang W" first="Wei" last="Wang">Wei Wang</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Tan, Yeqing" sort="Tan, Yeqing" uniqKey="Tan Y" first="Yeqing" last="Tan">Yeqing Tan</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Liu, Dandan" sort="Liu, Dandan" uniqKey="Liu D" first="Dandan" last="Liu">Dandan Liu</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Ma, Xujun" sort="Ma, Xujun" uniqKey="Ma X" first="Xujun" last="Ma">Xujun Ma</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Hou, Peichen" sort="Hou, Peichen" uniqKey="Hou P" first="Peichen" last="Hou">Peichen Hou</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Wang, Meijuan" sort="Wang, Meijuan" uniqKey="Wang M" first="Meijuan" last="Wang">Meijuan Wang</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Lu, Cunfu" sort="Lu, Cunfu" uniqKey="Lu C" first="Cunfu" last="Lu">Cunfu Lu</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Shen, Xin" sort="Shen, Xin" uniqKey="Shen X" first="Xin" last="Shen">Xin Shen</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Chen, Shaoliang" sort="Chen, Shaoliang" uniqKey="Chen S" first="Shaoliang" last="Chen">Shaoliang Chen</name>
<affiliation><nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.) lschen@bjfu.edu.cn.</nlm:affiliation>
</affiliation>
</author>
</analytic>
<series><title level="j">Plant physiology</title>
<idno type="eISSN">1532-2548</idno>
<imprint><date when="2015" type="published">2015</date>
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<term>Adenosine Triphosphatases (antagonists & inhibitors)</term>
<term>Adenosine Triphosphate (metabolism)</term>
<term>Apyrase (antagonists & inhibitors)</term>
<term>Apyrase (metabolism)</term>
<term>Arabidopsis (drug effects)</term>
<term>Arabidopsis (genetics)</term>
<term>Arabidopsis (physiology)</term>
<term>Cations, Divalent (pharmacology)</term>
<term>Cell Survival (drug effects)</term>
<term>Cold Temperature (MeSH)</term>
<term>Enzyme Inhibitors (pharmacology)</term>
<term>Extracellular Space (chemistry)</term>
<term>Hydrolysis (MeSH)</term>
<term>Plant Proteins (metabolism)</term>
<term>Plant Roots (cytology)</term>
<term>Plant Roots (drug effects)</term>
<term>Plant Roots (metabolism)</term>
<term>Plants, Genetically Modified (MeSH)</term>
<term>Populus (enzymology)</term>
<term>Protein Transport (drug effects)</term>
<term>Recombinant Proteins (metabolism)</term>
<term>Stress, Physiological (drug effects)</term>
<term>Subcellular Fractions (drug effects)</term>
<term>Subcellular Fractions (metabolism)</term>
<term>Substrate Specificity (drug effects)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="antagonists & inhibitors" xml:lang="en"><term>Adenosine Triphosphatases</term>
<term>Apyrase</term>
</keywords>
<keywords scheme="MESH" qualifier="chemistry" xml:lang="en"><term>Extracellular Space</term>
</keywords>
<keywords scheme="MESH" qualifier="cytology" xml:lang="en"><term>Plant Roots</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Adaptation, Physiological</term>
<term>Arabidopsis</term>
<term>Cell Survival</term>
<term>Plant Roots</term>
<term>Protein Transport</term>
<term>Stress, Physiological</term>
<term>Subcellular Fractions</term>
<term>Substrate Specificity</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en"><term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Arabidopsis</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Adenosine Triphosphate</term>
<term>Apyrase</term>
<term>Plant Proteins</term>
<term>Plant Roots</term>
<term>Recombinant Proteins</term>
<term>Subcellular Fractions</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Cations, Divalent</term>
<term>Enzyme Inhibitors</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Arabidopsis</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Cold Temperature</term>
<term>Hydrolysis</term>
<term>Plants, Genetically Modified</term>
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<front><div type="abstract" xml:lang="en">Apyrase and extracellular ATP play crucial roles in mediating plant growth and defense responses. In the cold-tolerant poplar, Populus euphratica, low temperatures up-regulate APYRASE2 (PeAPY2) expression in callus cells. We investigated the biochemical characteristics of PeAPY2 and its role in cold tolerance. We found that PeAPY2 predominantly localized to the plasma membrane, but punctate signals also appeared in the endoplasmic reticulum and Golgi apparatus. PeAPY2 exhibited broad substrate specificity, but it most efficiently hydrolyzed purine nucleotides, particularly ATP. PeAPY2 preferred Mg(2+) as a cofactor, and it was insensitive to various, specific ATPase inhibitors. When PeAPY2 was ectopically expressed in Arabidopsis (Arabidopsis thaliana), cold tolerance was enhanced, based on root growth measurements and survival rates. Moreover, under cold stress, PeAPY2-transgenic plants maintained plasma membrane integrity and showed reduced cold-elicited electrolyte leakage compared with wild-type plants. These responses probably resulted from efficient plasma membrane repair via vesicular trafficking. Indeed, transgenic plants showed accelerated endocytosis and exocytosis during cold stress and recovery. We found that low doses of extracellular ATP accelerated vesicular trafficking, but high extracellular ATP inhibited trafficking and reduced cell viability. Cold stress caused significant increases in root medium extracellular ATP. However, under these conditions, PeAPY2-transgenic lines showed greater control of extracellular ATP levels than wild-type plants. We conclude that Arabidopsis plants that overexpressed PeAPY2 could increase membrane repair by accelerating vesicular trafficking and hydrolyzing extracellular ATP to avoid excessive, cold-elicited ATP accumulation in the root medium and, thus, reduced ATP-induced inhibition of vesicular trafficking. </div>
</front>
</TEI>
<pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">26224801</PMID>
<DateCompleted><Year>2016</Year>
<Month>06</Month>
<Day>08</Day>
</DateCompleted>
<DateRevised><Year>2018</Year>
<Month>11</Month>
<Day>13</Day>
</DateRevised>
<Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1532-2548</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>169</Volume>
<Issue>1</Issue>
<PubDate><Year>2015</Year>
<Month>Sep</Month>
</PubDate>
</JournalIssue>
<Title>Plant physiology</Title>
<ISOAbbreviation>Plant Physiol</ISOAbbreviation>
</Journal>
<ArticleTitle>Populus euphratica APYRASE2 Enhances Cold Tolerance by Modulating Vesicular Trafficking and Extracellular ATP in Arabidopsis Plants.</ArticleTitle>
<Pagination><MedlinePgn>530-48</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1104/pp.15.00581</ELocationID>
<Abstract><AbstractText>Apyrase and extracellular ATP play crucial roles in mediating plant growth and defense responses. In the cold-tolerant poplar, Populus euphratica, low temperatures up-regulate APYRASE2 (PeAPY2) expression in callus cells. We investigated the biochemical characteristics of PeAPY2 and its role in cold tolerance. We found that PeAPY2 predominantly localized to the plasma membrane, but punctate signals also appeared in the endoplasmic reticulum and Golgi apparatus. PeAPY2 exhibited broad substrate specificity, but it most efficiently hydrolyzed purine nucleotides, particularly ATP. PeAPY2 preferred Mg(2+) as a cofactor, and it was insensitive to various, specific ATPase inhibitors. When PeAPY2 was ectopically expressed in Arabidopsis (Arabidopsis thaliana), cold tolerance was enhanced, based on root growth measurements and survival rates. Moreover, under cold stress, PeAPY2-transgenic plants maintained plasma membrane integrity and showed reduced cold-elicited electrolyte leakage compared with wild-type plants. These responses probably resulted from efficient plasma membrane repair via vesicular trafficking. Indeed, transgenic plants showed accelerated endocytosis and exocytosis during cold stress and recovery. We found that low doses of extracellular ATP accelerated vesicular trafficking, but high extracellular ATP inhibited trafficking and reduced cell viability. Cold stress caused significant increases in root medium extracellular ATP. However, under these conditions, PeAPY2-transgenic lines showed greater control of extracellular ATP levels than wild-type plants. We conclude that Arabidopsis plants that overexpressed PeAPY2 could increase membrane repair by accelerating vesicular trafficking and hydrolyzing extracellular ATP to avoid excessive, cold-elicited ATP accumulation in the root medium and, thus, reduced ATP-induced inhibition of vesicular trafficking. </AbstractText>
<CopyrightInformation>© 2015 American Society of Plant Biologists. All Rights Reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Deng</LastName>
<ForeName>Shurong</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Sun</LastName>
<ForeName>Jian</ForeName>
<Initials>J</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Zhao</LastName>
<ForeName>Rui</ForeName>
<Initials>R</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Ding</LastName>
<ForeName>Mingquan</ForeName>
<Initials>M</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-0835-6963</Identifier>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Zhang</LastName>
<ForeName>Yinan</ForeName>
<Initials>Y</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Sun</LastName>
<ForeName>Yuanling</ForeName>
<Initials>Y</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Wang</LastName>
<ForeName>Wei</ForeName>
<Initials>W</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y"><LastName>Tan</LastName>
<ForeName>Yeqing</ForeName>
<Initials>Y</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Liu</LastName>
<ForeName>Dandan</ForeName>
<Initials>D</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y"><LastName>Ma</LastName>
<ForeName>Xujun</ForeName>
<Initials>X</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y"><LastName>Hou</LastName>
<ForeName>Peichen</ForeName>
<Initials>P</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Wang</LastName>
<ForeName>Meijuan</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y"><LastName>Lu</LastName>
<ForeName>Cunfu</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y"><LastName>Shen</LastName>
<ForeName>Xin</ForeName>
<Initials>X</Initials>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Chen</LastName>
<ForeName>Shaoliang</ForeName>
<Initials>S</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-7511-3067</Identifier>
<AffiliationInfo><Affiliation>College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, People's Republic of China (S.D., R.Z., Y.Z., Y.S., W.W., Y.T., D.L., X.M., M.W., C.L., X.S., S.C.);College of Life Science, Jiangsu Normal University, Xuzhou 221116, People's Republic of China (J.S.);College of Agricultural and Food Science, Zhejiang Agricultural and Forestry University, Hangzhou 311300, People's Republic of China (M.D.); andNational Engineering Research Center for Information Technology in Agriculture, Beijing 100097, People's Republic of China (P.H.) lschen@bjfu.edu.cn.</Affiliation>
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<Language>eng</Language>
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<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2015</Year>
<Month>07</Month>
<Day>29</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>United States</Country>
<MedlineTA>Plant Physiol</MedlineTA>
<NlmUniqueID>0401224</NlmUniqueID>
<ISSNLinking>0032-0889</ISSNLinking>
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<NameOfSubstance UI="D004791">Enzyme Inhibitors</NameOfSubstance>
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<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
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<Chemical><RegistryNumber>0</RegistryNumber>
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<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D000251" MajorTopicYN="N">Adenosine Triphosphatases</DescriptorName>
<QualifierName UI="Q000037" MajorTopicYN="N">antagonists & inhibitors</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D000255" MajorTopicYN="N">Adenosine Triphosphate</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D001081" MajorTopicYN="N">Apyrase</DescriptorName>
<QualifierName UI="Q000037" MajorTopicYN="N">antagonists & inhibitors</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D017360" MajorTopicYN="N">Arabidopsis</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002413" MajorTopicYN="N">Cations, Divalent</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002470" MajorTopicYN="N">Cell Survival</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D003080" MajorTopicYN="Y">Cold Temperature</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D004791" MajorTopicYN="N">Enzyme Inhibitors</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D005110" MajorTopicYN="N">Extracellular Space</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D006868" MajorTopicYN="N">Hydrolysis</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D018517" MajorTopicYN="N">Plant Roots</DescriptorName>
<QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D030821" MajorTopicYN="N">Plants, Genetically Modified</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D021381" MajorTopicYN="N">Protein Transport</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D011994" MajorTopicYN="N">Recombinant Proteins</DescriptorName>
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</MeshHeading>
<MeshHeading><DescriptorName UI="D013312" MajorTopicYN="N">Stress, Physiological</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D013347" MajorTopicYN="N">Subcellular Fractions</DescriptorName>
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<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D013379" MajorTopicYN="N">Substrate Specificity</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
</MeshHeading>
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<PubMedPubDate PubStatus="accepted"><Year>2015</Year>
<Month>07</Month>
<Day>28</Day>
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Populus euphratica APYRASE2 Enhances Cold Tolerance by Modulating Vesicular Trafficking and Extracellular ATP in Arabidopsis Plants.

Populus euphratica APYRASE2 Enhances Cold Tolerance by Modulating Vesicular Trafficking and Extracellular ATP in Arabidopsis Plants.

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