Nitric oxide negatively regulates AKT1-mediated potassium uptake through modulating vitamin B6 homeostasis in Arabidopsis
Nitric oxide (NO), an active signaling molecule in plants, is involved in numerous physiological processes and adaptive responses to environmental stresses. Under high-salt conditions, plants accumulate NO quickly, and reorganize Na ⁺ and K ⁺ contents. However, the molecular connection between NO an...
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creator | Xia, Jinchan Kong, Dongdong Xue, Shaowu Tian, Wang Li, Nan Bao, Fang Hu, Yong Du, Jing Wang, Yu Pan, Xiaojun Wang, Lei Zhang, Xiaochen Niu, Guoqi Feng, Xue Li, Legong He, Yikun |
description | Nitric oxide (NO), an active signaling molecule in plants, is involved in numerous physiological processes and adaptive responses to environmental stresses. Under high-salt conditions, plants accumulate NO quickly, and reorganize Na ⁺ and K ⁺ contents. However, the molecular connection between NO and ion homeostasis is largely unknown. Here, we report that NO lowers K ⁺ channel AKT1-mediated plant K ⁺ uptake by modulating vitamin B6 biosynthesis. In a screen for Arabidopsis NO-hypersensitive mutants, we isolated sno1 ( sensitive to nitric oxide 1 ), which is allelic to the previously noted mutant sos4 ( salt overly sensitive 4 ) that has impaired Na ⁺ and K ⁺ contents and overproduces pyridoxal 5′-phosphate (PLP), an active form of vitamin B6. We showed that NO increased PLP and decreased K ⁺ levels in plant. NO induced SNO1 gene expression and enzyme activity, indicating that NO-triggered PLP accumulation mainly occurs through SNO1-mediated vitamin B6 salvage biosynthetic pathway. Furthermore, we demonstrated that PLP significantly repressed the activity of K ⁺ channel AKT1 in the Xenopus oocyte system and Arabidopsis root protoplasts. Together, our results suggest that NO decreases K ⁺ absorption by promoting the synthesis of vitamin B6 PLP, which further represses the activity of K ⁺ channel AKT1 in Arabidopsis . These findings reveal a previously unidentified pivotal role of NO in modulating the homeostasis of vitamin B6 and potassium nutrition in plants, and shed light on the mechanism of NO in plant acclimation to environmental changes.
Significance Nitric oxide (NO) plays key roles in coordinating plant growth and development with environmental cues. Potassium (K ⁺) is an essential plant nutrient important for growth and stress tolerance. However, little is known about the molecular connection of NO to K ⁺ homeostasis. Through a genetic approach, this study provides a detailed regulatory mechanism of NO to K ⁺ channel AKT1-mediated K ⁺ absorption, through its modulation on vitamin B6 biosynthesis in plants. This finding demonstrates a previously unidentified role of NO in the control of K ⁺ content in plants, which may represent a normal plant adaptive response under unfavorable external conditions. |
doi_str_mv | 10.1073/pnas.1417473111 |
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Significance Nitric oxide (NO) plays key roles in coordinating plant growth and development with environmental cues. Potassium (K ⁺) is an essential plant nutrient important for growth and stress tolerance. However, little is known about the molecular connection of NO to K ⁺ homeostasis. Through a genetic approach, this study provides a detailed regulatory mechanism of NO to K ⁺ channel AKT1-mediated K ⁺ absorption, through its modulation on vitamin B6 biosynthesis in plants. This finding demonstrates a previously unidentified role of NO in the control of K ⁺ content in plants, which may represent a normal plant adaptive response under unfavorable external conditions.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1417473111</identifier><identifier>PMID: 25355908</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>absorption ; Animals ; Arabidopsis ; Arabidopsis - cytology ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins ; Biological Sciences ; biosynthesis ; Electric current ; Flowers & plants ; Gene expression ; Gene expression regulation ; growth and development ; Homeostasis ; Homeostasis - physiology ; Ion Transport - physiology ; Molecules ; Nitric oxide ; Nitric Oxide - genetics ; Nitric Oxide - metabolism ; Oocytes ; Oxides ; plant growth ; Plant roots ; Plant Roots - cytology ; Plant Roots - metabolism ; Plants ; Potassium ; Potassium - metabolism ; Potassium Channels ; Protoplasts - cytology ; Protoplasts - metabolism ; Pyridoxal Phosphate - genetics ; Pyridoxal Phosphate - metabolism ; pyridoxine ; Salts ; Seedlings ; stress tolerance ; Vitamin B ; Vitamin B 6 - biosynthesis ; Vitamin B 6 - genetics ; Xenopus ; Xenopus laevis</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2014-11, Vol.111 (45), p.16196-16201</ispartof><rights>copyright © 1993–2008 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Nov 11, 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c558t-eaf4b484a51a1c00d3ce54944d16c2a34691ae465933281eea051db564ec57573</citedby><cites>FETCH-LOGICAL-c558t-eaf4b484a51a1c00d3ce54944d16c2a34691ae465933281eea051db564ec57573</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/111/45.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/43279233$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/43279233$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27903,27904,53769,53771,57995,58228</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25355908$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xia, Jinchan</creatorcontrib><creatorcontrib>Kong, Dongdong</creatorcontrib><creatorcontrib>Xue, Shaowu</creatorcontrib><creatorcontrib>Tian, Wang</creatorcontrib><creatorcontrib>Li, Nan</creatorcontrib><creatorcontrib>Bao, Fang</creatorcontrib><creatorcontrib>Hu, Yong</creatorcontrib><creatorcontrib>Du, Jing</creatorcontrib><creatorcontrib>Wang, Yu</creatorcontrib><creatorcontrib>Pan, Xiaojun</creatorcontrib><creatorcontrib>Wang, Lei</creatorcontrib><creatorcontrib>Zhang, Xiaochen</creatorcontrib><creatorcontrib>Niu, Guoqi</creatorcontrib><creatorcontrib>Feng, Xue</creatorcontrib><creatorcontrib>Li, Legong</creatorcontrib><creatorcontrib>He, Yikun</creatorcontrib><title>Nitric oxide negatively regulates AKT1-mediated potassium uptake through modulating vitamin B6 homeostasis in Arabidopsis</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Nitric oxide (NO), an active signaling molecule in plants, is involved in numerous physiological processes and adaptive responses to environmental stresses. Under high-salt conditions, plants accumulate NO quickly, and reorganize Na ⁺ and K ⁺ contents. However, the molecular connection between NO and ion homeostasis is largely unknown. Here, we report that NO lowers K ⁺ channel AKT1-mediated plant K ⁺ uptake by modulating vitamin B6 biosynthesis. In a screen for Arabidopsis NO-hypersensitive mutants, we isolated sno1 ( sensitive to nitric oxide 1 ), which is allelic to the previously noted mutant sos4 ( salt overly sensitive 4 ) that has impaired Na ⁺ and K ⁺ contents and overproduces pyridoxal 5′-phosphate (PLP), an active form of vitamin B6. We showed that NO increased PLP and decreased K ⁺ levels in plant. NO induced SNO1 gene expression and enzyme activity, indicating that NO-triggered PLP accumulation mainly occurs through SNO1-mediated vitamin B6 salvage biosynthetic pathway. Furthermore, we demonstrated that PLP significantly repressed the activity of K ⁺ channel AKT1 in the Xenopus oocyte system and Arabidopsis root protoplasts. Together, our results suggest that NO decreases K ⁺ absorption by promoting the synthesis of vitamin B6 PLP, which further represses the activity of K ⁺ channel AKT1 in Arabidopsis . These findings reveal a previously unidentified pivotal role of NO in modulating the homeostasis of vitamin B6 and potassium nutrition in plants, and shed light on the mechanism of NO in plant acclimation to environmental changes.
Significance Nitric oxide (NO) plays key roles in coordinating plant growth and development with environmental cues. Potassium (K ⁺) is an essential plant nutrient important for growth and stress tolerance. However, little is known about the molecular connection of NO to K ⁺ homeostasis. Through a genetic approach, this study provides a detailed regulatory mechanism of NO to K ⁺ channel AKT1-mediated K ⁺ absorption, through its modulation on vitamin B6 biosynthesis in plants. This finding demonstrates a previously unidentified role of NO in the control of K ⁺ content in plants, which may represent a normal plant adaptive response under unfavorable external conditions.</description><subject>absorption</subject><subject>Animals</subject><subject>Arabidopsis</subject><subject>Arabidopsis - cytology</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins</subject><subject>Biological Sciences</subject><subject>biosynthesis</subject><subject>Electric current</subject><subject>Flowers & plants</subject><subject>Gene expression</subject><subject>Gene expression regulation</subject><subject>growth and development</subject><subject>Homeostasis</subject><subject>Homeostasis - physiology</subject><subject>Ion Transport - physiology</subject><subject>Molecules</subject><subject>Nitric oxide</subject><subject>Nitric Oxide - genetics</subject><subject>Nitric Oxide - metabolism</subject><subject>Oocytes</subject><subject>Oxides</subject><subject>plant growth</subject><subject>Plant roots</subject><subject>Plant Roots - cytology</subject><subject>Plant Roots - metabolism</subject><subject>Plants</subject><subject>Potassium</subject><subject>Potassium - metabolism</subject><subject>Potassium Channels</subject><subject>Protoplasts - cytology</subject><subject>Protoplasts - metabolism</subject><subject>Pyridoxal Phosphate - genetics</subject><subject>Pyridoxal Phosphate - metabolism</subject><subject>pyridoxine</subject><subject>Salts</subject><subject>Seedlings</subject><subject>stress tolerance</subject><subject>Vitamin B</subject><subject>Vitamin B 6 - biosynthesis</subject><subject>Vitamin B 6 - genetics</subject><subject>Xenopus</subject><subject>Xenopus laevis</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNksuP0zAQxiMEYpfCmRNgiQuX7M74kdgXpLLiJVZwYPdsuYmbuiRx1k4q-t_jqKU8LnCyxvP7PntGX5Y9RbhAKNnl0Jt4gRxLXjJEvJedIyjMC67gfnYOQMtccsrPskcxbgFACQkPszMqmBAK5Hm2_-zG4Criv7vakt42ZnQ72-5JsM3UmtFGsvx0g3lna5eqmgx-NDG6qSPTMJpvloyb4KdmQzpfzwLXN2TnRtO5nrwpyMZ31sckcZGkm2UwK1f7IZWPswdr00b75Hgustt3b2-uPuTXX95_vFpe55UQcsytWfMVl9wINFgB1KyygivOaywqahgvFBrLC6EYoxKtNSCwXomC20qUomSL7PXBd5hWaYrK9mMwrR6C60zYa2-c_rPTu41u_E5zyniySQavjgbB3002jrpzsbJta3rrp6hRAgMFIMW_0YIppQoui_9AKVeMFhIT-vIvdOun0KelzZRgpSzTFxbZ5YGqgo8x2PVpRAQ9h0XPYdG_wpIUz3_fzIn_mY4EkCMwK092iJqL9DSqeYxnB2QbRx9ODGe0VJSx1H9x6K-N16YJLurbrxSwAEAOWJbsB5lC2Qw</recordid><startdate>20141111</startdate><enddate>20141111</enddate><creator>Xia, Jinchan</creator><creator>Kong, Dongdong</creator><creator>Xue, Shaowu</creator><creator>Tian, Wang</creator><creator>Li, Nan</creator><creator>Bao, Fang</creator><creator>Hu, Yong</creator><creator>Du, Jing</creator><creator>Wang, Yu</creator><creator>Pan, Xiaojun</creator><creator>Wang, Lei</creator><creator>Zhang, Xiaochen</creator><creator>Niu, Guoqi</creator><creator>Feng, Xue</creator><creator>Li, Legong</creator><creator>He, Yikun</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7ST</scope><scope>SOI</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20141111</creationdate><title>Nitric oxide negatively regulates AKT1-mediated potassium uptake through modulating vitamin B6 homeostasis in Arabidopsis</title><author>Xia, Jinchan ; Kong, Dongdong ; Xue, Shaowu ; Tian, Wang ; Li, Nan ; Bao, Fang ; Hu, Yong ; Du, Jing ; Wang, Yu ; Pan, Xiaojun ; Wang, Lei ; Zhang, Xiaochen ; Niu, Guoqi ; Feng, Xue ; Li, Legong ; He, Yikun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c558t-eaf4b484a51a1c00d3ce54944d16c2a34691ae465933281eea051db564ec57573</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>absorption</topic><topic>Animals</topic><topic>Arabidopsis</topic><topic>Arabidopsis - 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metabolism</topic><topic>pyridoxine</topic><topic>Salts</topic><topic>Seedlings</topic><topic>stress tolerance</topic><topic>Vitamin B</topic><topic>Vitamin B 6 - biosynthesis</topic><topic>Vitamin B 6 - genetics</topic><topic>Xenopus</topic><topic>Xenopus laevis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xia, Jinchan</creatorcontrib><creatorcontrib>Kong, Dongdong</creatorcontrib><creatorcontrib>Xue, Shaowu</creatorcontrib><creatorcontrib>Tian, Wang</creatorcontrib><creatorcontrib>Li, Nan</creatorcontrib><creatorcontrib>Bao, Fang</creatorcontrib><creatorcontrib>Hu, Yong</creatorcontrib><creatorcontrib>Du, Jing</creatorcontrib><creatorcontrib>Wang, Yu</creatorcontrib><creatorcontrib>Pan, Xiaojun</creatorcontrib><creatorcontrib>Wang, Lei</creatorcontrib><creatorcontrib>Zhang, Xiaochen</creatorcontrib><creatorcontrib>Niu, Guoqi</creatorcontrib><creatorcontrib>Feng, Xue</creatorcontrib><creatorcontrib>Li, Legong</creatorcontrib><creatorcontrib>He, Yikun</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>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Environment Abstracts</collection><collection>Environment Abstracts</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xia, Jinchan</au><au>Kong, Dongdong</au><au>Xue, Shaowu</au><au>Tian, Wang</au><au>Li, Nan</au><au>Bao, Fang</au><au>Hu, Yong</au><au>Du, Jing</au><au>Wang, Yu</au><au>Pan, Xiaojun</au><au>Wang, Lei</au><au>Zhang, Xiaochen</au><au>Niu, Guoqi</au><au>Feng, Xue</au><au>Li, Legong</au><au>He, Yikun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Nitric oxide negatively regulates AKT1-mediated potassium uptake through modulating vitamin B6 homeostasis in Arabidopsis</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2014-11-11</date><risdate>2014</risdate><volume>111</volume><issue>45</issue><spage>16196</spage><epage>16201</epage><pages>16196-16201</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Nitric oxide (NO), an active signaling molecule in plants, is involved in numerous physiological processes and adaptive responses to environmental stresses. Under high-salt conditions, plants accumulate NO quickly, and reorganize Na ⁺ and K ⁺ contents. However, the molecular connection between NO and ion homeostasis is largely unknown. Here, we report that NO lowers K ⁺ channel AKT1-mediated plant K ⁺ uptake by modulating vitamin B6 biosynthesis. In a screen for Arabidopsis NO-hypersensitive mutants, we isolated sno1 ( sensitive to nitric oxide 1 ), which is allelic to the previously noted mutant sos4 ( salt overly sensitive 4 ) that has impaired Na ⁺ and K ⁺ contents and overproduces pyridoxal 5′-phosphate (PLP), an active form of vitamin B6. We showed that NO increased PLP and decreased K ⁺ levels in plant. NO induced SNO1 gene expression and enzyme activity, indicating that NO-triggered PLP accumulation mainly occurs through SNO1-mediated vitamin B6 salvage biosynthetic pathway. Furthermore, we demonstrated that PLP significantly repressed the activity of K ⁺ channel AKT1 in the Xenopus oocyte system and Arabidopsis root protoplasts. Together, our results suggest that NO decreases K ⁺ absorption by promoting the synthesis of vitamin B6 PLP, which further represses the activity of K ⁺ channel AKT1 in Arabidopsis . These findings reveal a previously unidentified pivotal role of NO in modulating the homeostasis of vitamin B6 and potassium nutrition in plants, and shed light on the mechanism of NO in plant acclimation to environmental changes.
Significance Nitric oxide (NO) plays key roles in coordinating plant growth and development with environmental cues. Potassium (K ⁺) is an essential plant nutrient important for growth and stress tolerance. However, little is known about the molecular connection of NO to K ⁺ homeostasis. Through a genetic approach, this study provides a detailed regulatory mechanism of NO to K ⁺ channel AKT1-mediated K ⁺ absorption, through its modulation on vitamin B6 biosynthesis in plants. This finding demonstrates a previously unidentified role of NO in the control of K ⁺ content in plants, which may represent a normal plant adaptive response under unfavorable external conditions.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>25355908</pmid><doi>10.1073/pnas.1417473111</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | absorption Animals Arabidopsis Arabidopsis - cytology Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins Biological Sciences biosynthesis Electric current Flowers & plants Gene expression Gene expression regulation growth and development Homeostasis Homeostasis - physiology Ion Transport - physiology Molecules Nitric oxide Nitric Oxide - genetics Nitric Oxide - metabolism Oocytes Oxides plant growth Plant roots Plant Roots - cytology Plant Roots - metabolism Plants Potassium Potassium - metabolism Potassium Channels Protoplasts - cytology Protoplasts - metabolism Pyridoxal Phosphate - genetics Pyridoxal Phosphate - metabolism pyridoxine Salts Seedlings stress tolerance Vitamin B Vitamin B 6 - biosynthesis Vitamin B 6 - genetics Xenopus Xenopus laevis |
title | Nitric oxide negatively regulates AKT1-mediated potassium uptake through modulating vitamin B6 homeostasis in Arabidopsis |
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