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Downregulating VAC14 in Guard Cells Causes Drought Hypersensitivity by Inhibiting Stomatal Closure
Stomata are a key land plant innovation that permit the regulation of gaseous exchanges between the plant interior and the surrounding environment. By opening or closing, stomata regulate transpiration of water though the plant; and these actions are coordinated with acquisition of CO for photosynth...
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Published in: | Frontiers in plant science 2020-12, Vol.11, p.602701-602701 |
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description | Stomata are a key land plant innovation that permit the regulation of gaseous exchanges between the plant interior and the surrounding environment. By opening or closing, stomata regulate transpiration of water though the plant; and these actions are coordinated with acquisition of CO
for photosynthesis. Stomatal movement is controlled by various environmental and physiological factors and associates with multiple intracellular activities, among which the dynamic remodeling of vacuoles plays a crucial role. Phosphatidylinositol 3,5-bisphosphate [PI(3,5)P
] is critical for dynamic remodeling of vacuoles. Its production requires a PI(3,5)P
-metabolizing complex consisting of FAB1/PIKfyve kinases, SAC phosphatases, and the scaffolding protein VAC14. Although genetic or pharmacological downregulation of PI(3,5)P
causes hyposensitivity to ABA-induced stomatal closure, whether the effect of PI(3,5)P
on stomatal movement is cell-autonomous and the physiological consequences of its reduction were unclear. We report that downregulating Arabidopsis
specifically in guard cells by artificial microRNAs (amiR-VAC14) results in enlarged guard cells and hyposensitivity to ABA- and dark-induced stomatal closure. Vacuolar fission during stomatal closure is compromised by downregulating
in guard cells. Exogenous application of PI(3,5)P
rescued the amiR-VAC14 phenotype whereas PI(3,5)P
inhibitor YM201636 caused wild-type plants to have inhibited stomatal closure. We further show that downregulating VAC14 specifically in guard cells impairs drought tolerance, suggestive of a key role of guard cell-produced PI(3,5)P
in plant fitness. |
doi_str_mv | 10.3389/fpls.2020.602701 |
format | article |
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for photosynthesis. Stomatal movement is controlled by various environmental and physiological factors and associates with multiple intracellular activities, among which the dynamic remodeling of vacuoles plays a crucial role. Phosphatidylinositol 3,5-bisphosphate [PI(3,5)P
] is critical for dynamic remodeling of vacuoles. Its production requires a PI(3,5)P
-metabolizing complex consisting of FAB1/PIKfyve kinases, SAC phosphatases, and the scaffolding protein VAC14. Although genetic or pharmacological downregulation of PI(3,5)P
causes hyposensitivity to ABA-induced stomatal closure, whether the effect of PI(3,5)P
on stomatal movement is cell-autonomous and the physiological consequences of its reduction were unclear. We report that downregulating Arabidopsis
specifically in guard cells by artificial microRNAs (amiR-VAC14) results in enlarged guard cells and hyposensitivity to ABA- and dark-induced stomatal closure. Vacuolar fission during stomatal closure is compromised by downregulating
in guard cells. Exogenous application of PI(3,5)P
rescued the amiR-VAC14 phenotype whereas PI(3,5)P
inhibitor YM201636 caused wild-type plants to have inhibited stomatal closure. We further show that downregulating VAC14 specifically in guard cells impairs drought tolerance, suggestive of a key role of guard cell-produced PI(3,5)P
in plant fitness.</description><identifier>ISSN: 1664-462X</identifier><identifier>EISSN: 1664-462X</identifier><identifier>DOI: 10.3389/fpls.2020.602701</identifier><identifier>PMID: 33391314</identifier><language>eng</language><publisher>Switzerland: Frontiers Media S.A</publisher><subject>5)P2 ; ABA ; drought ; guard cell ; Plant Science ; vacuole fission</subject><ispartof>Frontiers in plant science, 2020-12, Vol.11, p.602701-602701</ispartof><rights>Copyright © 2020 Wang, Liu, Wu, Li, He, Zhang and Li.</rights><rights>Copyright © 2020 Wang, Liu, Wu, Li, He, Zhang and Li. 2020 Wang, Liu, Wu, Li, He, Zhang and Li</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c462t-73d61b6c0cd3f99c9325cdc9584d2a0e2b80a9c0968886ad1a6e80cb04a530bf3</citedby><cites>FETCH-LOGICAL-c462t-73d61b6c0cd3f99c9325cdc9584d2a0e2b80a9c0968886ad1a6e80cb04a530bf3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7773697/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7773697/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33391314$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Zong-Qi</creatorcontrib><creatorcontrib>Liu, Qi</creatorcontrib><creatorcontrib>Wu, Ju-Hua</creatorcontrib><creatorcontrib>Li, Juan</creatorcontrib><creatorcontrib>He, Jun-Min</creatorcontrib><creatorcontrib>Zhang, Yan</creatorcontrib><creatorcontrib>Li, Sha</creatorcontrib><title>Downregulating VAC14 in Guard Cells Causes Drought Hypersensitivity by Inhibiting Stomatal Closure</title><title>Frontiers in plant science</title><addtitle>Front Plant Sci</addtitle><description>Stomata are a key land plant innovation that permit the regulation of gaseous exchanges between the plant interior and the surrounding environment. By opening or closing, stomata regulate transpiration of water though the plant; and these actions are coordinated with acquisition of CO
for photosynthesis. Stomatal movement is controlled by various environmental and physiological factors and associates with multiple intracellular activities, among which the dynamic remodeling of vacuoles plays a crucial role. Phosphatidylinositol 3,5-bisphosphate [PI(3,5)P
] is critical for dynamic remodeling of vacuoles. Its production requires a PI(3,5)P
-metabolizing complex consisting of FAB1/PIKfyve kinases, SAC phosphatases, and the scaffolding protein VAC14. Although genetic or pharmacological downregulation of PI(3,5)P
causes hyposensitivity to ABA-induced stomatal closure, whether the effect of PI(3,5)P
on stomatal movement is cell-autonomous and the physiological consequences of its reduction were unclear. We report that downregulating Arabidopsis
specifically in guard cells by artificial microRNAs (amiR-VAC14) results in enlarged guard cells and hyposensitivity to ABA- and dark-induced stomatal closure. Vacuolar fission during stomatal closure is compromised by downregulating
in guard cells. Exogenous application of PI(3,5)P
rescued the amiR-VAC14 phenotype whereas PI(3,5)P
inhibitor YM201636 caused wild-type plants to have inhibited stomatal closure. We further show that downregulating VAC14 specifically in guard cells impairs drought tolerance, suggestive of a key role of guard cell-produced PI(3,5)P
in plant fitness.</description><subject>5)P2</subject><subject>ABA</subject><subject>drought</subject><subject>guard cell</subject><subject>Plant Science</subject><subject>vacuole fission</subject><issn>1664-462X</issn><issn>1664-462X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNpVkUtP3DAQgKOqqCDg3lPlYy-7jB9x7EslFFpYCamHQtWb5VeyRtl4aztU---bZQHBXDyyZ74Z-auqzxiWlAp50W2HvCRAYMmBNIA_VCeYc7ZgnPz5-CY_rs5zfoA5agApm0_VMaVUYorZSWWu4r8x-X4adAljj35ftpihMKLrSSeHWj8MGbV6yj6jqxSnfl3QzW7rU_ZjDiU8hrJDZodW4zqY8IT4VeJGFz2gdoh5Sv6sOur0kP3583la3f_4ftfeLG5_Xq_ay9uFnbcsi4Y6jg23YB3tpLSSkto6K2vBHNHgiRGgpQXJhRBcO6y5F2ANMF1TMB09rVYHrov6QW1T2Oi0U1EH9XQRU690KsEOXnkHhmLOGkckE5gYzogQIETnuas5nVnfDqztZDbeWT-WpId30PcvY1irPj6qpmkol80M-PoMSPHv5HNRm5Dt_Jt69HHKirCmBlELXM-lcCi1KeacfPc6BoPam1Z702pvWh1Mzy1f3q732vDilf4HDL2lwg</recordid><startdate>20201217</startdate><enddate>20201217</enddate><creator>Wang, Zong-Qi</creator><creator>Liu, Qi</creator><creator>Wu, Ju-Hua</creator><creator>Li, Juan</creator><creator>He, Jun-Min</creator><creator>Zhang, Yan</creator><creator>Li, Sha</creator><general>Frontiers Media S.A</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20201217</creationdate><title>Downregulating VAC14 in Guard Cells Causes Drought Hypersensitivity by Inhibiting Stomatal Closure</title><author>Wang, Zong-Qi ; Liu, Qi ; Wu, Ju-Hua ; Li, Juan ; He, Jun-Min ; Zhang, Yan ; Li, Sha</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c462t-73d61b6c0cd3f99c9325cdc9584d2a0e2b80a9c0968886ad1a6e80cb04a530bf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>5)P2</topic><topic>ABA</topic><topic>drought</topic><topic>guard cell</topic><topic>Plant Science</topic><topic>vacuole fission</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Zong-Qi</creatorcontrib><creatorcontrib>Liu, Qi</creatorcontrib><creatorcontrib>Wu, Ju-Hua</creatorcontrib><creatorcontrib>Li, Juan</creatorcontrib><creatorcontrib>He, Jun-Min</creatorcontrib><creatorcontrib>Zhang, Yan</creatorcontrib><creatorcontrib>Li, Sha</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Frontiers in plant science</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Zong-Qi</au><au>Liu, Qi</au><au>Wu, Ju-Hua</au><au>Li, Juan</au><au>He, Jun-Min</au><au>Zhang, Yan</au><au>Li, Sha</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Downregulating VAC14 in Guard Cells Causes Drought Hypersensitivity by Inhibiting Stomatal Closure</atitle><jtitle>Frontiers in plant science</jtitle><addtitle>Front Plant Sci</addtitle><date>2020-12-17</date><risdate>2020</risdate><volume>11</volume><spage>602701</spage><epage>602701</epage><pages>602701-602701</pages><issn>1664-462X</issn><eissn>1664-462X</eissn><abstract>Stomata are a key land plant innovation that permit the regulation of gaseous exchanges between the plant interior and the surrounding environment. By opening or closing, stomata regulate transpiration of water though the plant; and these actions are coordinated with acquisition of CO
for photosynthesis. Stomatal movement is controlled by various environmental and physiological factors and associates with multiple intracellular activities, among which the dynamic remodeling of vacuoles plays a crucial role. Phosphatidylinositol 3,5-bisphosphate [PI(3,5)P
] is critical for dynamic remodeling of vacuoles. Its production requires a PI(3,5)P
-metabolizing complex consisting of FAB1/PIKfyve kinases, SAC phosphatases, and the scaffolding protein VAC14. Although genetic or pharmacological downregulation of PI(3,5)P
causes hyposensitivity to ABA-induced stomatal closure, whether the effect of PI(3,5)P
on stomatal movement is cell-autonomous and the physiological consequences of its reduction were unclear. We report that downregulating Arabidopsis
specifically in guard cells by artificial microRNAs (amiR-VAC14) results in enlarged guard cells and hyposensitivity to ABA- and dark-induced stomatal closure. Vacuolar fission during stomatal closure is compromised by downregulating
in guard cells. Exogenous application of PI(3,5)P
rescued the amiR-VAC14 phenotype whereas PI(3,5)P
inhibitor YM201636 caused wild-type plants to have inhibited stomatal closure. We further show that downregulating VAC14 specifically in guard cells impairs drought tolerance, suggestive of a key role of guard cell-produced PI(3,5)P
in plant fitness.</abstract><cop>Switzerland</cop><pub>Frontiers Media S.A</pub><pmid>33391314</pmid><doi>10.3389/fpls.2020.602701</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 5)P2 ABA drought guard cell Plant Science vacuole fission |
title | Downregulating VAC14 in Guard Cells Causes Drought Hypersensitivity by Inhibiting Stomatal Closure |
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