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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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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