Receptor-Like Kinase RUPO Interacts with Potassium Transporters to Regulate Pollen Tube Growth and Integrity in Rice
During sexual reproduction of flowering plants, the pollen tube grows fast and over a long distance within the pistil to deliver two sperms for double fertilization. Growing plant cells need to communicate constantly with external stimuli as well as monitor changes in surface tension of the cell wal...
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description | During sexual reproduction of flowering plants, the pollen tube grows fast and over a long distance within the pistil to deliver two sperms for double fertilization. Growing plant cells need to communicate constantly with external stimuli as well as monitor changes in surface tension of the cell wall and plasma membrane to coordinate these signals and internal growth machinery; however, the underlying mechanisms remain largely unknown. Here we show that the rice member of plant-specific receptor-like kinase CrRLK1Ls subfamily, Ruptured Pollen tube (RUPO), is specifically expressed in rice pollen. RUPO localizes to the apical plasma membrane and vesicle of pollen tubes and is required for male gamete transmission. K+ levels were greater in pollen of homozygous CRISPR-knockout lines than wild-type plants, and pollen tubes burst shortly after germination. We reveal the interaction of RUPO with high-affinity potassium transporters. Phosphorylation of RUPO established and dephosphorylation abolished the interaction. These results have revealed the receptor-like kinase as a regulator of high-affinity potassium transporters via phosphorylation-dependent interaction, and demonstrated a novel receptor-like kinase signaling pathway that mediates K+ homeostasis required for pollen tube growth and integrity. |
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Growing plant cells need to communicate constantly with external stimuli as well as monitor changes in surface tension of the cell wall and plasma membrane to coordinate these signals and internal growth machinery; however, the underlying mechanisms remain largely unknown. Here we show that the rice member of plant-specific receptor-like kinase CrRLK1Ls subfamily, Ruptured Pollen tube (RUPO), is specifically expressed in rice pollen. RUPO localizes to the apical plasma membrane and vesicle of pollen tubes and is required for male gamete transmission. K+ levels were greater in pollen of homozygous CRISPR-knockout lines than wild-type plants, and pollen tubes burst shortly after germination. We reveal the interaction of RUPO with high-affinity potassium transporters. Phosphorylation of RUPO established and dephosphorylation abolished the interaction. These results have revealed the receptor-like kinase as a regulator of high-affinity potassium transporters via phosphorylation-dependent interaction, and demonstrated a novel receptor-like kinase signaling pathway that mediates K+ homeostasis required for pollen tube growth and integrity.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1006085</identifier><identifier>PMID: 27447945</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Arabidopsis - genetics ; Arabidopsis Proteins - genetics ; Biology and Life Sciences ; Flowers - genetics ; Flowers - growth & development ; Gene Expression Regulation, Plant ; Genetic aspects ; Germination ; Germination - genetics ; Growth ; Homeostasis ; Kinases ; Localization ; Magnoliopsida - genetics ; Magnoliopsida - growth & development ; Medicine and Health Sciences ; Membrane Proteins - biosynthesis ; Membrane Proteins - genetics ; Microscopy ; Observations ; Oryza - genetics ; Oryza - growth & development ; Phosphorylation ; Phosphotransferases ; Physiological aspects ; Plant Proteins - genetics ; Plant reproduction ; Pollen ; Pollen - genetics ; Pollen - growth & development ; Pollen Tube - genetics ; Pollen Tube - growth & development ; Pollination - genetics ; Potassium ; Potassium channels ; Potassium-Hydrogen Antiporters - biosynthesis ; Potassium-Hydrogen Antiporters - genetics ; Protein Kinases - genetics ; Protein-protein interactions ; Receptor Protein-Tyrosine Kinases - genetics ; Research and Analysis Methods ; Rice ; Sperm</subject><ispartof>PLoS genetics, 2016-07, Vol.12 (7), p.e1006085-e1006085</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Liu L, Zheng C, Kuang B, Wei L, Yan L, Wang T (2016) Receptor-Like Kinase RUPO Interacts with Potassium Transporters to Regulate Pollen Tube Growth and Integrity in Rice. PLoS Genet 12(7): e1006085. doi:10.1371/journal.pgen.1006085</rights><rights>2016 Liu et al 2016 Liu et al</rights><rights>2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Liu L, Zheng C, Kuang B, Wei L, Yan L, Wang T (2016) Receptor-Like Kinase RUPO Interacts with Potassium Transporters to Regulate Pollen Tube Growth and Integrity in Rice. PLoS Genet 12(7): e1006085. doi:10.1371/journal.pgen.1006085</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c829t-da5681312c5f0b32255242a6362656f3e55c05f7d72458aaa2e70207820516e83</citedby><cites>FETCH-LOGICAL-c829t-da5681312c5f0b32255242a6362656f3e55c05f7d72458aaa2e70207820516e83</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/PMC4957769/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4957769/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27447945$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Lingtong</creatorcontrib><creatorcontrib>Zheng, Canhui</creatorcontrib><creatorcontrib>Kuang, Baijan</creatorcontrib><creatorcontrib>Wei, Liqin</creatorcontrib><creatorcontrib>Yan, Longfeng</creatorcontrib><creatorcontrib>Wang, Tai</creatorcontrib><title>Receptor-Like Kinase RUPO Interacts with Potassium Transporters to Regulate Pollen Tube Growth and Integrity in Rice</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>During sexual reproduction of flowering plants, the pollen tube grows fast and over a long distance within the pistil to deliver two sperms for double fertilization. Growing plant cells need to communicate constantly with external stimuli as well as monitor changes in surface tension of the cell wall and plasma membrane to coordinate these signals and internal growth machinery; however, the underlying mechanisms remain largely unknown. Here we show that the rice member of plant-specific receptor-like kinase CrRLK1Ls subfamily, Ruptured Pollen tube (RUPO), is specifically expressed in rice pollen. RUPO localizes to the apical plasma membrane and vesicle of pollen tubes and is required for male gamete transmission. K+ levels were greater in pollen of homozygous CRISPR-knockout lines than wild-type plants, and pollen tubes burst shortly after germination. We reveal the interaction of RUPO with high-affinity potassium transporters. Phosphorylation of RUPO established and dephosphorylation abolished the interaction. These results have revealed the receptor-like kinase as a regulator of high-affinity potassium transporters via phosphorylation-dependent interaction, and demonstrated a novel receptor-like kinase signaling pathway that mediates K+ homeostasis required for pollen tube growth and integrity.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Biology and Life Sciences</subject><subject>Flowers - genetics</subject><subject>Flowers - growth & development</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genetic aspects</subject><subject>Germination</subject><subject>Germination - genetics</subject><subject>Growth</subject><subject>Homeostasis</subject><subject>Kinases</subject><subject>Localization</subject><subject>Magnoliopsida - genetics</subject><subject>Magnoliopsida - growth & development</subject><subject>Medicine and Health Sciences</subject><subject>Membrane Proteins - biosynthesis</subject><subject>Membrane Proteins - genetics</subject><subject>Microscopy</subject><subject>Observations</subject><subject>Oryza - genetics</subject><subject>Oryza - growth & development</subject><subject>Phosphorylation</subject><subject>Phosphotransferases</subject><subject>Physiological aspects</subject><subject>Plant Proteins - genetics</subject><subject>Plant reproduction</subject><subject>Pollen</subject><subject>Pollen - genetics</subject><subject>Pollen - growth & development</subject><subject>Pollen Tube - genetics</subject><subject>Pollen Tube - growth & development</subject><subject>Pollination - genetics</subject><subject>Potassium</subject><subject>Potassium channels</subject><subject>Potassium-Hydrogen Antiporters - biosynthesis</subject><subject>Potassium-Hydrogen Antiporters - genetics</subject><subject>Protein Kinases - genetics</subject><subject>Protein-protein interactions</subject><subject>Receptor Protein-Tyrosine Kinases - genetics</subject><subject>Research and Analysis Methods</subject><subject>Rice</subject><subject>Sperm</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVk9Fu0zAUhiMEYmPwBggiISG4aLGdOE5ukKYJRkVFp9Jxa7nOSerh2sV2GHt73DabGrSLIV_Ysr__9_E5PknyEqMxzhj-cGU7Z4Qeb1owY4xQgUr6KDnGlGYjlqP88cH6KHnm_RVCGS0r9jQ5IizPWZXT4yTMQcImWDeaqp-QflVGeEjnlxezdGICOCGDT69VWKUXNgjvVbdOF04Yv7EuHvs02HQObadFgIhoDSZddEtIz529jiph6p1R61S4SZVJ50rC8-RJI7SHF_18klx-_rQ4-zKazs4nZ6fTkSxJFUa1oEWJM0wkbdAyI4RSkhNRZAUpaNFkQKlEtGE1IzkthRAEGCKIlQRRXECZnSSv974bbT3vE-Y5LjGpqgyjIhKTPVFbccU3Tq2Fu-FWKL7bsK7lwgUlNXCJWIMhFzEanDMGYlnVGFC9bCpKyp3Xx_62brmGWoIJTuiB6fDEqBVv7W-eV5SxoooG73oDZ3914ANfKy9Ba2HAdru4KUOozMoHoIiRWGGydX3zD3p_InqqFfGtyjQ2hii3pvx0-1UYwwWJ1PgeKo4a1kpaA42K-wPB-4EgMgH-hFZ03vPJ9_l_sN8ezs5-DNm3B-wKhA4rb3UXlDV-COZ7UDrrvYPmrnYY8W3P3WaOb3uO9z0XZa8O634num2y7C_S-iQL</recordid><startdate>20160701</startdate><enddate>20160701</enddate><creator>Liu, Lingtong</creator><creator>Zheng, Canhui</creator><creator>Kuang, Baijan</creator><creator>Wei, Liqin</creator><creator>Yan, Longfeng</creator><creator>Wang, Tai</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160701</creationdate><title>Receptor-Like Kinase RUPO Interacts with Potassium Transporters to Regulate Pollen Tube Growth and Integrity in Rice</title><author>Liu, Lingtong ; Zheng, Canhui ; Kuang, Baijan ; Wei, Liqin ; Yan, Longfeng ; Wang, Tai</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c829t-da5681312c5f0b32255242a6362656f3e55c05f7d72458aaa2e70207820516e83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Arabidopsis - genetics</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Biology and Life Sciences</topic><topic>Flowers - genetics</topic><topic>Flowers - growth & development</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genetic aspects</topic><topic>Germination</topic><topic>Germination - genetics</topic><topic>Growth</topic><topic>Homeostasis</topic><topic>Kinases</topic><topic>Localization</topic><topic>Magnoliopsida - genetics</topic><topic>Magnoliopsida - growth & development</topic><topic>Medicine and Health Sciences</topic><topic>Membrane Proteins - biosynthesis</topic><topic>Membrane Proteins - genetics</topic><topic>Microscopy</topic><topic>Observations</topic><topic>Oryza - genetics</topic><topic>Oryza - growth & development</topic><topic>Phosphorylation</topic><topic>Phosphotransferases</topic><topic>Physiological aspects</topic><topic>Plant Proteins - genetics</topic><topic>Plant reproduction</topic><topic>Pollen</topic><topic>Pollen - genetics</topic><topic>Pollen - growth & development</topic><topic>Pollen Tube - genetics</topic><topic>Pollen Tube - growth & development</topic><topic>Pollination - genetics</topic><topic>Potassium</topic><topic>Potassium channels</topic><topic>Potassium-Hydrogen Antiporters - biosynthesis</topic><topic>Potassium-Hydrogen Antiporters - genetics</topic><topic>Protein Kinases - genetics</topic><topic>Protein-protein interactions</topic><topic>Receptor Protein-Tyrosine Kinases - genetics</topic><topic>Research and Analysis Methods</topic><topic>Rice</topic><topic>Sperm</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Lingtong</creatorcontrib><creatorcontrib>Zheng, Canhui</creatorcontrib><creatorcontrib>Kuang, Baijan</creatorcontrib><creatorcontrib>Wei, Liqin</creatorcontrib><creatorcontrib>Yan, Longfeng</creatorcontrib><creatorcontrib>Wang, Tai</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Lingtong</au><au>Zheng, Canhui</au><au>Kuang, Baijan</au><au>Wei, Liqin</au><au>Yan, Longfeng</au><au>Wang, Tai</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Receptor-Like Kinase RUPO Interacts with Potassium Transporters to Regulate Pollen Tube Growth and Integrity in Rice</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2016-07-01</date><risdate>2016</risdate><volume>12</volume><issue>7</issue><spage>e1006085</spage><epage>e1006085</epage><pages>e1006085-e1006085</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>During sexual reproduction of flowering plants, the pollen tube grows fast and over a long distance within the pistil to deliver two sperms for double fertilization. Growing plant cells need to communicate constantly with external stimuli as well as monitor changes in surface tension of the cell wall and plasma membrane to coordinate these signals and internal growth machinery; however, the underlying mechanisms remain largely unknown. Here we show that the rice member of plant-specific receptor-like kinase CrRLK1Ls subfamily, Ruptured Pollen tube (RUPO), is specifically expressed in rice pollen. RUPO localizes to the apical plasma membrane and vesicle of pollen tubes and is required for male gamete transmission. K+ levels were greater in pollen of homozygous CRISPR-knockout lines than wild-type plants, and pollen tubes burst shortly after germination. We reveal the interaction of RUPO with high-affinity potassium transporters. Phosphorylation of RUPO established and dephosphorylation abolished the interaction. These results have revealed the receptor-like kinase as a regulator of high-affinity potassium transporters via phosphorylation-dependent interaction, and demonstrated a novel receptor-like kinase signaling pathway that mediates K+ homeostasis required for pollen tube growth and integrity.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27447945</pmid><doi>10.1371/journal.pgen.1006085</doi><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis - genetics Arabidopsis Proteins - genetics Biology and Life Sciences Flowers - genetics Flowers - growth & development Gene Expression Regulation, Plant Genetic aspects Germination Germination - genetics Growth Homeostasis Kinases Localization Magnoliopsida - genetics Magnoliopsida - growth & development Medicine and Health Sciences Membrane Proteins - biosynthesis Membrane Proteins - genetics Microscopy Observations Oryza - genetics Oryza - growth & development Phosphorylation Phosphotransferases Physiological aspects Plant Proteins - genetics Plant reproduction Pollen Pollen - genetics Pollen - growth & development Pollen Tube - genetics Pollen Tube - growth & development Pollination - genetics Potassium Potassium channels Potassium-Hydrogen Antiporters - biosynthesis Potassium-Hydrogen Antiporters - genetics Protein Kinases - genetics Protein-protein interactions Receptor Protein-Tyrosine Kinases - genetics Research and Analysis Methods Rice Sperm |
title | Receptor-Like Kinase RUPO Interacts with Potassium Transporters to Regulate Pollen Tube Growth and Integrity in Rice |
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