The Rice Receptor-Like Kinases DWARF AND RUNTISH SPIKELET1 and 2 Repress Cell Death and Affect Sugar Utilization during Reproductive Development
Cell-to-cell communication precisely controls the creation of new organs during reproductive growth. However, the sensor molecules that mediate developmental signals in monocot plants are poorly understood. Here, we report that DWARF AND RUNTISH SPIKELET1 (DRUS1) and DRUS2, two closely related recep...
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creator | Pu, Cui-Xia Han, Yong-Feng Zhu, Shu Song, Feng-Yan Zhao, Ying Wang, Chun-Yan Zhang, Yong-Cun Yang, Qian Wang, Jiao Bu, Shuo-Lei Sun, Li-Jing Zhang, Sheng-Wei Zhang, Su-Qiao Sun, Da-Ye Sun, Ying |
description | Cell-to-cell communication precisely controls the creation of new organs during reproductive growth. However, the sensor molecules that mediate developmental signals in monocot plants are poorly understood. Here, we report that DWARF AND RUNTISH SPIKELET1 (DRUS1) and DRUS2, two closely related receptor-like kinases (RLKs), redundantly control reproductive growth and development in rice (Oryza sativa). A drus1-1 drus2 double knockout mutant, but not either single mutant, showed extreme dwarfism and barren inflorescences that harbored sterile spikelets. The gibberellin pathway was not impaired in this mutant. A phenotypic comparison of mutants expressing different amounts of DRUS1 and 2 revealed that reproductive growth requires a threshold level of DRUS1/2 proteins. DRUS1 and 2 maintain cell viability by repressing protease-mediated cell degradation and likely by affecting sugar utilization or conversion. In the later stages of anther development, survival of the endothecium requires DRUS1/2, which may stimulate expression of the UDP-glucose pyrophosphorylase gene UGP2 and starch biosynthesis in pollen. Unlike their Arabidopsis thaliana ortholog FERONIA, DRUS1 and 2 mediate a fundamental signaling process that is essential for cell survival and represents a novel biological function for the CrRLK1L RLK subfamily. |
doi_str_mv | 10.1105/tpc.16.00218 |
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However, the sensor molecules that mediate developmental signals in monocot plants are poorly understood. Here, we report that DWARF AND RUNTISH SPIKELET1 (DRUS1) and DRUS2, two closely related receptor-like kinases (RLKs), redundantly control reproductive growth and development in rice (Oryza sativa). A drus1-1 drus2 double knockout mutant, but not either single mutant, showed extreme dwarfism and barren inflorescences that harbored sterile spikelets. The gibberellin pathway was not impaired in this mutant. A phenotypic comparison of mutants expressing different amounts of DRUS1 and 2 revealed that reproductive growth requires a threshold level of DRUS1/2 proteins. DRUS1 and 2 maintain cell viability by repressing protease-mediated cell degradation and likely by affecting sugar utilization or conversion. In the later stages of anther development, survival of the endothecium requires DRUS1/2, which may stimulate expression of the UDP-glucose pyrophosphorylase gene UGP2 and starch biosynthesis in pollen. Unlike their Arabidopsis thaliana ortholog FERONIA, DRUS1 and 2 mediate a fundamental signaling process that is essential for cell survival and represents a novel biological function for the CrRLK1L RLK subfamily.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.16.00218</identifier><identifier>PMID: 28082384</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Amino Acid Sequence ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Biosynthesis ; Carbohydrate Metabolism - genetics ; Cell death ; Cell Death - genetics ; Cell interactions ; Cell survival ; Developmental stages ; Dwarfism ; Endothecium ; Flowers - enzymology ; Flowers - genetics ; Flowers - ultrastructure ; Gene expression ; Gene Expression Profiling - methods ; Gene Expression Regulation, Plant ; Immunoblotting ; In Situ Hybridization ; Kinases ; Microscopy, Confocal ; Microscopy, Electron ; Mutants ; Organs ; Oryza - enzymology ; Oryza - genetics ; Oryza sativa ; Phosphotransferases - genetics ; Phosphotransferases - metabolism ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants, Genetically Modified ; Pollen ; Proteins ; Receptor Protein-Tyrosine Kinases - genetics ; Receptor Protein-Tyrosine Kinases - metabolism ; Reproduction - genetics ; RNA Interference ; Sequence Homology, Amino Acid ; Signaling ; Starch ; Starch - metabolism ; Sugar ; Survival</subject><ispartof>The Plant cell, 2017-01, Vol.29 (1), p.70-89</ispartof><rights>2017 American Society of Plant Biologists</rights><rights>2017 American Society of Plant Biologists. All rights reserved.</rights><rights>Copyright American Society of Plant Biologists Jan 2017</rights><rights>2017 American Society of Plant Biologists. All rights reserved. 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c467t-f9041e6cad770269f9cc84d99e8dd4f836b920dac3848e3057a8da8e780a39723</citedby><orcidid>0000-0002-1444-5057 ; 0000-0002-5626-668X ; 0000-0001-5460-8925 ; 0000-0001-6308-8511</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/90000566$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/90000566$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,27901,27902,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28082384$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Pu, Cui-Xia</creatorcontrib><creatorcontrib>Han, Yong-Feng</creatorcontrib><creatorcontrib>Zhu, Shu</creatorcontrib><creatorcontrib>Song, Feng-Yan</creatorcontrib><creatorcontrib>Zhao, Ying</creatorcontrib><creatorcontrib>Wang, Chun-Yan</creatorcontrib><creatorcontrib>Zhang, Yong-Cun</creatorcontrib><creatorcontrib>Yang, Qian</creatorcontrib><creatorcontrib>Wang, Jiao</creatorcontrib><creatorcontrib>Bu, Shuo-Lei</creatorcontrib><creatorcontrib>Sun, Li-Jing</creatorcontrib><creatorcontrib>Zhang, Sheng-Wei</creatorcontrib><creatorcontrib>Zhang, Su-Qiao</creatorcontrib><creatorcontrib>Sun, Da-Ye</creatorcontrib><creatorcontrib>Sun, Ying</creatorcontrib><title>The Rice Receptor-Like Kinases DWARF AND RUNTISH SPIKELET1 and 2 Repress Cell Death and Affect Sugar Utilization during Reproductive Development</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>Cell-to-cell communication precisely controls the creation of new organs during reproductive growth. However, the sensor molecules that mediate developmental signals in monocot plants are poorly understood. Here, we report that DWARF AND RUNTISH SPIKELET1 (DRUS1) and DRUS2, two closely related receptor-like kinases (RLKs), redundantly control reproductive growth and development in rice (Oryza sativa). A drus1-1 drus2 double knockout mutant, but not either single mutant, showed extreme dwarfism and barren inflorescences that harbored sterile spikelets. The gibberellin pathway was not impaired in this mutant. A phenotypic comparison of mutants expressing different amounts of DRUS1 and 2 revealed that reproductive growth requires a threshold level of DRUS1/2 proteins. DRUS1 and 2 maintain cell viability by repressing protease-mediated cell degradation and likely by affecting sugar utilization or conversion. In the later stages of anther development, survival of the endothecium requires DRUS1/2, which may stimulate expression of the UDP-glucose pyrophosphorylase gene UGP2 and starch biosynthesis in pollen. Unlike their Arabidopsis thaliana ortholog FERONIA, DRUS1 and 2 mediate a fundamental signaling process that is essential for cell survival and represents a novel biological function for the CrRLK1L RLK subfamily.</description><subject>Amino Acid Sequence</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Biosynthesis</subject><subject>Carbohydrate Metabolism - genetics</subject><subject>Cell death</subject><subject>Cell Death - genetics</subject><subject>Cell interactions</subject><subject>Cell survival</subject><subject>Developmental stages</subject><subject>Dwarfism</subject><subject>Endothecium</subject><subject>Flowers - enzymology</subject><subject>Flowers - genetics</subject><subject>Flowers - ultrastructure</subject><subject>Gene expression</subject><subject>Gene Expression Profiling - methods</subject><subject>Gene Expression Regulation, Plant</subject><subject>Immunoblotting</subject><subject>In Situ Hybridization</subject><subject>Kinases</subject><subject>Microscopy, Confocal</subject><subject>Microscopy, Electron</subject><subject>Mutants</subject><subject>Organs</subject><subject>Oryza - enzymology</subject><subject>Oryza - genetics</subject><subject>Oryza sativa</subject><subject>Phosphotransferases - genetics</subject><subject>Phosphotransferases - metabolism</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants, Genetically Modified</subject><subject>Pollen</subject><subject>Proteins</subject><subject>Receptor Protein-Tyrosine Kinases - genetics</subject><subject>Receptor Protein-Tyrosine Kinases - metabolism</subject><subject>Reproduction - genetics</subject><subject>RNA Interference</subject><subject>Sequence Homology, Amino Acid</subject><subject>Signaling</subject><subject>Starch</subject><subject>Starch - metabolism</subject><subject>Sugar</subject><subject>Survival</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkk-P0zAQxSMEYpeFG1eQJS4cSBk7jmNfVqraLltttaD-Edwsr-O0Lmkc7KQSfAo-Mt52qYATF9vS-80bz-glyUsMA4whf9-1eoDZAIBg_ig5x3lGUiL4l8fxDRRSynJ8ljwLYQsAuMDiaXJGOHCScXqe_FxuDJpbHQ-jTds5n87sV4NubKOCCWj8eTi_QsPbMZqvbpfTxTVafJreTGaTJUaqKRGJda03IaCRqWs0NqrbHIRhVRndoUW_Vh6tOlvbH6qzrkFl722zPpS5sted3ZtYtje1a3em6Z4nTypVB_Pi4b5IVleT5eg6nX38MB0NZ6mmrOjSSgDFhmlVFgUQJiqhNaelEIaXJa14xu4EgVLpOCU3GeSF4qXipuCgMlGQ7CK5PPq2_d3OlDq29qqWrbc75b9Lp6z8W2nsRq7dXuYZ0IzSaPD2wcC7b70JndzZoOMSVGNcHyTmBeGYE8D_gTJMKaMFRPTNP-jW9b6Jm5AEgAmIfvfUuyOlvQvBm-r0bwzyPhUypkJiJg-piPjrP2c9wb9jEIFXR2AbYgJOuoiJgZyx7Be-dLrp</recordid><startdate>20170101</startdate><enddate>20170101</enddate><creator>Pu, Cui-Xia</creator><creator>Han, Yong-Feng</creator><creator>Zhu, Shu</creator><creator>Song, Feng-Yan</creator><creator>Zhao, Ying</creator><creator>Wang, Chun-Yan</creator><creator>Zhang, Yong-Cun</creator><creator>Yang, Qian</creator><creator>Wang, Jiao</creator><creator>Bu, Shuo-Lei</creator><creator>Sun, Li-Jing</creator><creator>Zhang, Sheng-Wei</creator><creator>Zhang, Su-Qiao</creator><creator>Sun, Da-Ye</creator><creator>Sun, Ying</creator><general>American Society of Plant Biologists</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>4T-</scope><scope>7QO</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1444-5057</orcidid><orcidid>https://orcid.org/0000-0002-5626-668X</orcidid><orcidid>https://orcid.org/0000-0001-5460-8925</orcidid><orcidid>https://orcid.org/0000-0001-6308-8511</orcidid></search><sort><creationdate>20170101</creationdate><title>The Rice Receptor-Like Kinases DWARF AND RUNTISH SPIKELET1 and 2 Repress Cell Death and Affect Sugar Utilization during Reproductive Development</title><author>Pu, Cui-Xia ; Han, Yong-Feng ; Zhu, Shu ; Song, Feng-Yan ; Zhao, Ying ; Wang, Chun-Yan ; Zhang, Yong-Cun ; Yang, Qian ; Wang, Jiao ; Bu, Shuo-Lei ; Sun, Li-Jing ; Zhang, Sheng-Wei ; Zhang, Su-Qiao ; Sun, Da-Ye ; Sun, Ying</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c467t-f9041e6cad770269f9cc84d99e8dd4f836b920dac3848e3057a8da8e780a39723</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Amino Acid Sequence</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Biosynthesis</topic><topic>Carbohydrate Metabolism - genetics</topic><topic>Cell death</topic><topic>Cell Death - genetics</topic><topic>Cell interactions</topic><topic>Cell survival</topic><topic>Developmental stages</topic><topic>Dwarfism</topic><topic>Endothecium</topic><topic>Flowers - enzymology</topic><topic>Flowers - genetics</topic><topic>Flowers - ultrastructure</topic><topic>Gene expression</topic><topic>Gene Expression Profiling - methods</topic><topic>Gene Expression Regulation, Plant</topic><topic>Immunoblotting</topic><topic>In Situ Hybridization</topic><topic>Kinases</topic><topic>Microscopy, Confocal</topic><topic>Microscopy, Electron</topic><topic>Mutants</topic><topic>Organs</topic><topic>Oryza - enzymology</topic><topic>Oryza - genetics</topic><topic>Oryza sativa</topic><topic>Phosphotransferases - genetics</topic><topic>Phosphotransferases - metabolism</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants, Genetically Modified</topic><topic>Pollen</topic><topic>Proteins</topic><topic>Receptor Protein-Tyrosine Kinases - genetics</topic><topic>Receptor Protein-Tyrosine Kinases - metabolism</topic><topic>Reproduction - genetics</topic><topic>RNA Interference</topic><topic>Sequence Homology, Amino Acid</topic><topic>Signaling</topic><topic>Starch</topic><topic>Starch - metabolism</topic><topic>Sugar</topic><topic>Survival</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pu, Cui-Xia</creatorcontrib><creatorcontrib>Han, Yong-Feng</creatorcontrib><creatorcontrib>Zhu, Shu</creatorcontrib><creatorcontrib>Song, Feng-Yan</creatorcontrib><creatorcontrib>Zhao, Ying</creatorcontrib><creatorcontrib>Wang, Chun-Yan</creatorcontrib><creatorcontrib>Zhang, Yong-Cun</creatorcontrib><creatorcontrib>Yang, Qian</creatorcontrib><creatorcontrib>Wang, Jiao</creatorcontrib><creatorcontrib>Bu, Shuo-Lei</creatorcontrib><creatorcontrib>Sun, Li-Jing</creatorcontrib><creatorcontrib>Zhang, Sheng-Wei</creatorcontrib><creatorcontrib>Zhang, Su-Qiao</creatorcontrib><creatorcontrib>Sun, Da-Ye</creatorcontrib><creatorcontrib>Sun, Ying</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Docstoc</collection><collection>Biotechnology Research Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Plant cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pu, Cui-Xia</au><au>Han, Yong-Feng</au><au>Zhu, Shu</au><au>Song, Feng-Yan</au><au>Zhao, Ying</au><au>Wang, Chun-Yan</au><au>Zhang, Yong-Cun</au><au>Yang, Qian</au><au>Wang, Jiao</au><au>Bu, Shuo-Lei</au><au>Sun, Li-Jing</au><au>Zhang, Sheng-Wei</au><au>Zhang, Su-Qiao</au><au>Sun, Da-Ye</au><au>Sun, Ying</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Rice Receptor-Like Kinases DWARF AND RUNTISH SPIKELET1 and 2 Repress Cell Death and Affect Sugar Utilization during Reproductive Development</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2017-01-01</date><risdate>2017</risdate><volume>29</volume><issue>1</issue><spage>70</spage><epage>89</epage><pages>70-89</pages><issn>1040-4651</issn><eissn>1532-298X</eissn><abstract>Cell-to-cell communication precisely controls the creation of new organs during reproductive growth. However, the sensor molecules that mediate developmental signals in monocot plants are poorly understood. Here, we report that DWARF AND RUNTISH SPIKELET1 (DRUS1) and DRUS2, two closely related receptor-like kinases (RLKs), redundantly control reproductive growth and development in rice (Oryza sativa). A drus1-1 drus2 double knockout mutant, but not either single mutant, showed extreme dwarfism and barren inflorescences that harbored sterile spikelets. The gibberellin pathway was not impaired in this mutant. A phenotypic comparison of mutants expressing different amounts of DRUS1 and 2 revealed that reproductive growth requires a threshold level of DRUS1/2 proteins. DRUS1 and 2 maintain cell viability by repressing protease-mediated cell degradation and likely by affecting sugar utilization or conversion. In the later stages of anther development, survival of the endothecium requires DRUS1/2, which may stimulate expression of the UDP-glucose pyrophosphorylase gene UGP2 and starch biosynthesis in pollen. Unlike their Arabidopsis thaliana ortholog FERONIA, DRUS1 and 2 mediate a fundamental signaling process that is essential for cell survival and represents a novel biological function for the CrRLK1L RLK subfamily.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>28082384</pmid><doi>10.1105/tpc.16.00218</doi><tpages>20</tpages><orcidid>https://orcid.org/0000-0002-1444-5057</orcidid><orcidid>https://orcid.org/0000-0002-5626-668X</orcidid><orcidid>https://orcid.org/0000-0001-5460-8925</orcidid><orcidid>https://orcid.org/0000-0001-6308-8511</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amino Acid Sequence Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Biosynthesis Carbohydrate Metabolism - genetics Cell death Cell Death - genetics Cell interactions Cell survival Developmental stages Dwarfism Endothecium Flowers - enzymology Flowers - genetics Flowers - ultrastructure Gene expression Gene Expression Profiling - methods Gene Expression Regulation, Plant Immunoblotting In Situ Hybridization Kinases Microscopy, Confocal Microscopy, Electron Mutants Organs Oryza - enzymology Oryza - genetics Oryza sativa Phosphotransferases - genetics Phosphotransferases - metabolism Plant Proteins - genetics Plant Proteins - metabolism Plants, Genetically Modified Pollen Proteins Receptor Protein-Tyrosine Kinases - genetics Receptor Protein-Tyrosine Kinases - metabolism Reproduction - genetics RNA Interference Sequence Homology, Amino Acid Signaling Starch Starch - metabolism Sugar Survival |
title | The Rice Receptor-Like Kinases DWARF AND RUNTISH SPIKELET1 and 2 Repress Cell Death and Affect Sugar Utilization during Reproductive Development |
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