Vacuolar Proton Pyrophosphatase Is Required for High Magnesium Tolerance in <i>Arabidopsis</i>

Magnesium (Mg<sup>2+</sup>) is an essential nutrient in all organisms. However, high levels of Mg<sup>2+</sup> in the environment are toxic to plants. In this study, we identified the vacuolar-type H<sup>+</sup>-pyrophosphatase, AVP1, as a critical enzyme for opti...

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Main Authors: Yang Yang, Ren-Jie Tang, Baicong Mu, Ali Ferjani, Jisen Shi, Hongxia Zhang, Fugeng Zhao, Wen-Zhi Lan, Sheng Luan
Format: Article
Language:English
Published: MDPI AG 2018-11-01
Series:International Journal of Molecular Sciences
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Online Access:https://www.mdpi.com/1422-0067/19/11/3617
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spelling doaj-bf65e52598ab4114a95cd73008938c722020-11-24T22:52:09ZengMDPI AGInternational Journal of Molecular Sciences1422-00672018-11-011911361710.3390/ijms19113617ijms19113617Vacuolar Proton Pyrophosphatase Is Required for High Magnesium Tolerance in <i>Arabidopsis</i>Yang Yang0Ren-Jie Tang1Baicong Mu2Ali Ferjani3Jisen Shi4Hongxia Zhang5Fugeng Zhao6Wen-Zhi Lan7Sheng Luan8Nanjing University-Nanjing Forestry University Joint Institute for Plant Molecular Biology, College of Life Sciences, Nanjing University, Nanjing 210093, ChinaDepartment of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USANanjing University-Nanjing Forestry University Joint Institute for Plant Molecular Biology, College of Life Sciences, Nanjing University, Nanjing 210093, ChinaDepartment of Biology, Tokyo Gakugei University, Koganei, Tokyo 184-8501, JapanNanjing University-Nanjing Forestry University Joint Institute for Plant Molecular Biology, Key Laboratory of Forest Genetics and Biotechnology, Nanjing Forestry University, Nanjing 210037, ChinaCollege of Agriculture, Ludong University, Yantai 264025, ChinaNanjing University-Nanjing Forestry University Joint Institute for Plant Molecular Biology, College of Life Sciences, Nanjing University, Nanjing 210093, ChinaNanjing University-Nanjing Forestry University Joint Institute for Plant Molecular Biology, College of Life Sciences, Nanjing University, Nanjing 210093, ChinaDepartment of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USAMagnesium (Mg<sup>2+</sup>) is an essential nutrient in all organisms. However, high levels of Mg<sup>2+</sup> in the environment are toxic to plants. In this study, we identified the vacuolar-type H<sup>+</sup>-pyrophosphatase, AVP1, as a critical enzyme for optimal plant growth under high-Mg conditions. The <i>Arabidopsis</i> <i>avp1</i> mutants displayed severe growth retardation, as compared to the wild-type plants upon excessive Mg<sup>2+</sup>. Unexpectedly, the <i>avp1</i> mutant plants retained similar Mg content to wild-type plants under either normal or high Mg conditions, suggesting that AVP1 may not directly contribute to Mg<sup>2+</sup> homeostasis in plant cells. Further analyses confirmed that the <i>avp1</i> mutant plants contained a higher pyrophosphate (PPi) content than wild type, coupled with impaired vacuolar H<sup>+</sup>-pyrophosphatase activity. Interestingly, expression of the <i>Saccharomyces cerevisiae</i> cytosolic inorganic pyrophosphatase1 gene <i>IPP1</i>, which facilitates PPi hydrolysis but not proton translocation into vacuole, rescued the growth defects of <i>avp1</i> mutants under high-Mg conditions. These results provide evidence that high-Mg sensitivity in <i>avp1</i> mutants possibly resulted from elevated level of cytosolic PPi. Moreover, genetic analysis indicated that mutation of <i>AVP1</i> was additive to the defects in <i>mgt6</i> and <i>cbl2 cbl3</i> mutants that are previously known to be impaired in Mg<sup>2+</sup> homeostasis. Taken together, our results suggest AVP1 is required for cellular PPi homeostasis that in turn contributes to high-Mg tolerance in plant cells.https://www.mdpi.com/1422-0067/19/11/3617vacuolar H<sup>+</sup>-pyrophosphatase<i>AtAVP1</i>cellular PPi homeostasishigh-Mg tolerance
collection DOAJ
language English
format Article
sources DOAJ
author Yang Yang
Ren-Jie Tang
Baicong Mu
Ali Ferjani
Jisen Shi
Hongxia Zhang
Fugeng Zhao
Wen-Zhi Lan
Sheng Luan
spellingShingle Yang Yang
Ren-Jie Tang
Baicong Mu
Ali Ferjani
Jisen Shi
Hongxia Zhang
Fugeng Zhao
Wen-Zhi Lan
Sheng Luan
Vacuolar Proton Pyrophosphatase Is Required for High Magnesium Tolerance in <i>Arabidopsis</i>
International Journal of Molecular Sciences
vacuolar H<sup>+</sup>-pyrophosphatase
<i>AtAVP1</i>
cellular PPi homeostasis
high-Mg tolerance
author_facet Yang Yang
Ren-Jie Tang
Baicong Mu
Ali Ferjani
Jisen Shi
Hongxia Zhang
Fugeng Zhao
Wen-Zhi Lan
Sheng Luan
author_sort Yang Yang
title Vacuolar Proton Pyrophosphatase Is Required for High Magnesium Tolerance in <i>Arabidopsis</i>
title_short Vacuolar Proton Pyrophosphatase Is Required for High Magnesium Tolerance in <i>Arabidopsis</i>
title_full Vacuolar Proton Pyrophosphatase Is Required for High Magnesium Tolerance in <i>Arabidopsis</i>
title_fullStr Vacuolar Proton Pyrophosphatase Is Required for High Magnesium Tolerance in <i>Arabidopsis</i>
title_full_unstemmed Vacuolar Proton Pyrophosphatase Is Required for High Magnesium Tolerance in <i>Arabidopsis</i>
title_sort vacuolar proton pyrophosphatase is required for high magnesium tolerance in <i>arabidopsis</i>
publisher MDPI AG
series International Journal of Molecular Sciences
issn 1422-0067
publishDate 2018-11-01
description Magnesium (Mg<sup>2+</sup>) is an essential nutrient in all organisms. However, high levels of Mg<sup>2+</sup> in the environment are toxic to plants. In this study, we identified the vacuolar-type H<sup>+</sup>-pyrophosphatase, AVP1, as a critical enzyme for optimal plant growth under high-Mg conditions. The <i>Arabidopsis</i> <i>avp1</i> mutants displayed severe growth retardation, as compared to the wild-type plants upon excessive Mg<sup>2+</sup>. Unexpectedly, the <i>avp1</i> mutant plants retained similar Mg content to wild-type plants under either normal or high Mg conditions, suggesting that AVP1 may not directly contribute to Mg<sup>2+</sup> homeostasis in plant cells. Further analyses confirmed that the <i>avp1</i> mutant plants contained a higher pyrophosphate (PPi) content than wild type, coupled with impaired vacuolar H<sup>+</sup>-pyrophosphatase activity. Interestingly, expression of the <i>Saccharomyces cerevisiae</i> cytosolic inorganic pyrophosphatase1 gene <i>IPP1</i>, which facilitates PPi hydrolysis but not proton translocation into vacuole, rescued the growth defects of <i>avp1</i> mutants under high-Mg conditions. These results provide evidence that high-Mg sensitivity in <i>avp1</i> mutants possibly resulted from elevated level of cytosolic PPi. Moreover, genetic analysis indicated that mutation of <i>AVP1</i> was additive to the defects in <i>mgt6</i> and <i>cbl2 cbl3</i> mutants that are previously known to be impaired in Mg<sup>2+</sup> homeostasis. Taken together, our results suggest AVP1 is required for cellular PPi homeostasis that in turn contributes to high-Mg tolerance in plant cells.
topic vacuolar H<sup>+</sup>-pyrophosphatase
<i>AtAVP1</i>
cellular PPi homeostasis
high-Mg tolerance
url https://www.mdpi.com/1422-0067/19/11/3617
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