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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Veröffentlicht in:Proceedings of the National Academy of Sciences - PNAS 2014-11, Vol.111 (45), p.16196-16201
Hauptverfasser: 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
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container_end_page 16201
container_issue 45
container_start_page 16196
container_title Proceedings of the National Academy of Sciences - PNAS
container_volume 111
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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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. 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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. 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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 - cytology</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins</topic><topic>Biological Sciences</topic><topic>biosynthesis</topic><topic>Electric current</topic><topic>Flowers &amp; plants</topic><topic>Gene expression</topic><topic>Gene expression regulation</topic><topic>growth and development</topic><topic>Homeostasis</topic><topic>Homeostasis - physiology</topic><topic>Ion Transport - physiology</topic><topic>Molecules</topic><topic>Nitric oxide</topic><topic>Nitric Oxide - genetics</topic><topic>Nitric Oxide - metabolism</topic><topic>Oocytes</topic><topic>Oxides</topic><topic>plant growth</topic><topic>Plant roots</topic><topic>Plant Roots - cytology</topic><topic>Plant Roots - metabolism</topic><topic>Plants</topic><topic>Potassium</topic><topic>Potassium - metabolism</topic><topic>Potassium Channels</topic><topic>Protoplasts - cytology</topic><topic>Protoplasts - metabolism</topic><topic>Pyridoxal Phosphate - genetics</topic><topic>Pyridoxal Phosphate - 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 &amp; 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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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source Jstor Complete Legacy; MEDLINE; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry
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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