The activation of OsEIL1 on YUC8 transcription and auxin biosynthesis is required for ethylene-inhibited root elongation in rice early seedling development
Rice is an important monocotyledonous crop worldwide; it differs from the dicotyledonous plant Arabidopsis in many aspects. In Arabidopsis, ethylene and auxin act synergistically to regulate root growth and development. However, their interaction in rice is still unclear. Here, we report that the tr...
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| description | Rice is an important monocotyledonous crop worldwide; it differs from the dicotyledonous plant Arabidopsis in many aspects. In Arabidopsis, ethylene and auxin act synergistically to regulate root growth and development. However, their interaction in rice is still unclear. Here, we report that the transcriptional activation of OsEIL1 on the expression of YUC8/REIN7 and indole-3-pyruvic acid (IPA)-dependent auxin biosynthesis is required for ethylene-inhibited root elongation. Using an inhibitor of YUC activity, which regulates auxin biosynthesis via the conversion of IPA to indole-3-acetic acid (IAA), we showed that ethylene-inhibited primary root elongation is dependent on YUC-based auxin biosynthesis. By screening phenotypes of seedling primary root from mutagenesis libraries following ethylene treatment, we identified a rice ethylene-insensitive mutant, rein7-1, in which YUC8/REIN7 is truncated at its C-terminus. Mutation in YUC8/REIN7 reduced auxin biosynthesis in rice, while YUC8/REIN7 overexpression enhanced ethylene sensitivity in the roots. Moreover, YUC8/REIN7 catalyzed the conversion of IPA to IAA, truncated version at C-terminal end of the YUC8/REIN7 resulted in significant reduction of enzymatic activity, indicating that YUC8/REIN7 is required for IPA-dependent auxin biosynthesis and ethylene-inhibited root elongation in rice early seedlings. Further investigations indicated that ethylene induced YUC8/REIN7 expression and promoted auxin accumulation in roots. Addition of low concentrations of IAA rescued the ethylene response in the rein7-1, strongly demonstrating that ethylene-inhibited root elongation depends on IPA-dependent auxin biosynthesis. Genetic studies revealed that YUC8/REIN7-mediated auxin biosynthesis functioned downstream of OsEIL1, which directly activated the expression of YUC8/REIN7. Thus, our findings reveal a model of interaction between ethylene and auxin in rice seedling primary root elongation, enhancing our understanding of ethylene signaling in rice. |
| doi_str_mv | 10.1371/journal.pgen.1006955 |
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In Arabidopsis, ethylene and auxin act synergistically to regulate root growth and development. However, their interaction in rice is still unclear. Here, we report that the transcriptional activation of OsEIL1 on the expression of YUC8/REIN7 and indole-3-pyruvic acid (IPA)-dependent auxin biosynthesis is required for ethylene-inhibited root elongation. Using an inhibitor of YUC activity, which regulates auxin biosynthesis via the conversion of IPA to indole-3-acetic acid (IAA), we showed that ethylene-inhibited primary root elongation is dependent on YUC-based auxin biosynthesis. By screening phenotypes of seedling primary root from mutagenesis libraries following ethylene treatment, we identified a rice ethylene-insensitive mutant, rein7-1, in which YUC8/REIN7 is truncated at its C-terminus. Mutation in YUC8/REIN7 reduced auxin biosynthesis in rice, while YUC8/REIN7 overexpression enhanced ethylene sensitivity in the roots. Moreover, YUC8/REIN7 catalyzed the conversion of IPA to IAA, truncated version at C-terminal end of the YUC8/REIN7 resulted in significant reduction of enzymatic activity, indicating that YUC8/REIN7 is required for IPA-dependent auxin biosynthesis and ethylene-inhibited root elongation in rice early seedlings. Further investigations indicated that ethylene induced YUC8/REIN7 expression and promoted auxin accumulation in roots. Addition of low concentrations of IAA rescued the ethylene response in the rein7-1, strongly demonstrating that ethylene-inhibited root elongation depends on IPA-dependent auxin biosynthesis. Genetic studies revealed that YUC8/REIN7-mediated auxin biosynthesis functioned downstream of OsEIL1, which directly activated the expression of YUC8/REIN7. Thus, our findings reveal a model of interaction between ethylene and auxin in rice seedling primary root elongation, enhancing our understanding of ethylene signaling in rice.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1006955</identifier><identifier>PMID: 28829777</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acetic acid ; Arabidopsis Proteins - genetics ; Biology and Life Sciences ; Biosynthesis ; Biotechnology ; C-Terminus ; Elongation ; Enzymatic activity ; Ethylene ; Ethylenes - metabolism ; Funding ; Gene Expression Regulation, Plant ; Genes ; Indole-3-pyruvic acid ; Indoleacetic acid ; Indoleacetic Acids - metabolism ; Indoles - metabolism ; Low concentrations ; Mixed Function Oxygenases - genetics ; Mutagenesis ; Mutation ; Oryza - genetics ; Oryza - growth & development ; Physical Sciences ; Plant Development - genetics ; Plant Growth Regulators - genetics ; Plant Roots - genetics ; Plant Roots - growth & development ; Plants, Genetically Modified - genetics ; Pyruvic acid ; R&D ; Research & development ; Research and Analysis Methods ; Rice ; Roots ; Seedlings ; Seedlings - genetics ; Seedlings - growth & development ; Sensitivity enhancement ; Software ; Transcription activation ; Transcription Factors - genetics</subject><ispartof>PLoS genetics, 2017-08, Vol.13 (8), p.e1006955</ispartof><rights>2017 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: transcription and auxin biosynthesis is required for ethylene-inhibited root elongation in rice early seedling development. PLoS Genet 13(8): e1006955. https://doi.org/10.1371/journal.pgen.1006955</rights><rights>2017 Qin et al 2017 Qin et al</rights><rights>2017 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: transcription and auxin biosynthesis is required for ethylene-inhibited root elongation in rice early seedling development. PLoS Genet 13(8): e1006955. https://doi.org/10.1371/journal.pgen.1006955</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4375-dc9f1b9106fa47aba311d347e26a50795bc5d1c5732ee884a3a5934967833acd3</citedby><cites>FETCH-LOGICAL-c4375-dc9f1b9106fa47aba311d347e26a50795bc5d1c5732ee884a3a5934967833acd3</cites><orcidid>0000-0001-9788-7290</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5581195/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5581195/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28829777$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Yu, Hao</contributor><creatorcontrib>Qin, Hua</creatorcontrib><creatorcontrib>Zhang, Zhijin</creatorcontrib><creatorcontrib>Wang, Juan</creatorcontrib><creatorcontrib>Chen, Xinbing</creatorcontrib><creatorcontrib>Wei, Pengcheng</creatorcontrib><creatorcontrib>Huang, Rongfeng</creatorcontrib><title>The activation of OsEIL1 on YUC8 transcription and auxin biosynthesis is required for ethylene-inhibited root elongation in rice early seedling development</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Rice is an important monocotyledonous crop worldwide; it differs from the dicotyledonous plant Arabidopsis in many aspects. In Arabidopsis, ethylene and auxin act synergistically to regulate root growth and development. However, their interaction in rice is still unclear. Here, we report that the transcriptional activation of OsEIL1 on the expression of YUC8/REIN7 and indole-3-pyruvic acid (IPA)-dependent auxin biosynthesis is required for ethylene-inhibited root elongation. Using an inhibitor of YUC activity, which regulates auxin biosynthesis via the conversion of IPA to indole-3-acetic acid (IAA), we showed that ethylene-inhibited primary root elongation is dependent on YUC-based auxin biosynthesis. By screening phenotypes of seedling primary root from mutagenesis libraries following ethylene treatment, we identified a rice ethylene-insensitive mutant, rein7-1, in which YUC8/REIN7 is truncated at its C-terminus. Mutation in YUC8/REIN7 reduced auxin biosynthesis in rice, while YUC8/REIN7 overexpression enhanced ethylene sensitivity in the roots. Moreover, YUC8/REIN7 catalyzed the conversion of IPA to IAA, truncated version at C-terminal end of the YUC8/REIN7 resulted in significant reduction of enzymatic activity, indicating that YUC8/REIN7 is required for IPA-dependent auxin biosynthesis and ethylene-inhibited root elongation in rice early seedlings. Further investigations indicated that ethylene induced YUC8/REIN7 expression and promoted auxin accumulation in roots. Addition of low concentrations of IAA rescued the ethylene response in the rein7-1, strongly demonstrating that ethylene-inhibited root elongation depends on IPA-dependent auxin biosynthesis. Genetic studies revealed that YUC8/REIN7-mediated auxin biosynthesis functioned downstream of OsEIL1, which directly activated the expression of YUC8/REIN7. Thus, our findings reveal a model of interaction between ethylene and auxin in rice seedling primary root elongation, enhancing our understanding of ethylene signaling in rice.</description><subject>Acetic acid</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Biology and Life Sciences</subject><subject>Biosynthesis</subject><subject>Biotechnology</subject><subject>C-Terminus</subject><subject>Elongation</subject><subject>Enzymatic activity</subject><subject>Ethylene</subject><subject>Ethylenes - metabolism</subject><subject>Funding</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Indole-3-pyruvic acid</subject><subject>Indoleacetic acid</subject><subject>Indoleacetic Acids - metabolism</subject><subject>Indoles - metabolism</subject><subject>Low concentrations</subject><subject>Mixed Function Oxygenases - genetics</subject><subject>Mutagenesis</subject><subject>Mutation</subject><subject>Oryza - genetics</subject><subject>Oryza - growth & development</subject><subject>Physical Sciences</subject><subject>Plant Development - genetics</subject><subject>Plant Growth Regulators - genetics</subject><subject>Plant Roots - genetics</subject><subject>Plant Roots - growth & development</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Pyruvic acid</subject><subject>R&D</subject><subject>Research & development</subject><subject>Research and Analysis Methods</subject><subject>Rice</subject><subject>Roots</subject><subject>Seedlings</subject><subject>Seedlings - genetics</subject><subject>Seedlings - growth & development</subject><subject>Sensitivity enhancement</subject><subject>Software</subject><subject>Transcription activation</subject><subject>Transcription Factors - genetics</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNp1Us1uGyEQXlWtmjTtG1QtUs92wcACl0qVlbaWLOWSHHpCszBrY23AgbVVP0tftiR2ouRQCQmY-X4G9DXNR0anjCv2dZN2OcIw3a4wThmlrZHyVXPOpOQTJah4_ex81rwrZUMpl9qot83ZTOuZUUqdN3-v10jAjWEPY0iRpJ5clcvFkpF6-X0z12TMEIvLYfvQh-gJ7P6ESLqQyiGOayyhkLoy3u1CRk_6lAmO68OAESchrkMXxlrOKY0EhxRXR6cqkYNDgpCHAymIfghxRTzuK2h7i3F837zpYSj44bRfNDc_Lq_nvybLq5-L-fflxAmu5MQ707POMNr2IBR0wBnzXCictSCpMrJz0jMnFZ8hai2AgzRcmFZpzsF5ftF8Pupuh1Ts6V-LZYYbwXWFVsTiiPAJNnabwy3kg00Q7EMh5ZWFPAY3oJVeYKsNYyCd8EgBupZR3QKdmc4ZVrW-ndx23S16Vx-aYXgh-rITw9qu0t5KqRkzsgp8OQnkdLfDMv5nZHFEuZxKydg_OTBq7wP0yLL3AbKnAFXap-fTPZEeE8P_AeVKx3k</recordid><startdate>201708</startdate><enddate>201708</enddate><creator>Qin, Hua</creator><creator>Zhang, Zhijin</creator><creator>Wang, Juan</creator><creator>Chen, Xinbing</creator><creator>Wei, Pengcheng</creator><creator>Huang, Rongfeng</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>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>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-9788-7290</orcidid></search><sort><creationdate>201708</creationdate><title>The activation of OsEIL1 on YUC8 transcription and auxin biosynthesis is required for ethylene-inhibited root elongation in rice early seedling development</title><author>Qin, Hua ; Zhang, Zhijin ; Wang, Juan ; Chen, Xinbing ; Wei, Pengcheng ; Huang, Rongfeng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4375-dc9f1b9106fa47aba311d347e26a50795bc5d1c5732ee884a3a5934967833acd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Acetic acid</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Biology and Life Sciences</topic><topic>Biosynthesis</topic><topic>Biotechnology</topic><topic>C-Terminus</topic><topic>Elongation</topic><topic>Enzymatic activity</topic><topic>Ethylene</topic><topic>Ethylenes - metabolism</topic><topic>Funding</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genes</topic><topic>Indole-3-pyruvic acid</topic><topic>Indoleacetic acid</topic><topic>Indoleacetic Acids - metabolism</topic><topic>Indoles - metabolism</topic><topic>Low concentrations</topic><topic>Mixed Function Oxygenases - genetics</topic><topic>Mutagenesis</topic><topic>Mutation</topic><topic>Oryza - genetics</topic><topic>Oryza - growth & development</topic><topic>Physical Sciences</topic><topic>Plant Development - genetics</topic><topic>Plant Growth Regulators - genetics</topic><topic>Plant Roots - genetics</topic><topic>Plant Roots - growth & development</topic><topic>Plants, Genetically Modified - genetics</topic><topic>Pyruvic acid</topic><topic>R&D</topic><topic>Research & development</topic><topic>Research and Analysis Methods</topic><topic>Rice</topic><topic>Roots</topic><topic>Seedlings</topic><topic>Seedlings - genetics</topic><topic>Seedlings - growth & development</topic><topic>Sensitivity enhancement</topic><topic>Software</topic><topic>Transcription activation</topic><topic>Transcription Factors - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Qin, Hua</creatorcontrib><creatorcontrib>Zhang, Zhijin</creatorcontrib><creatorcontrib>Wang, Juan</creatorcontrib><creatorcontrib>Chen, Xinbing</creatorcontrib><creatorcontrib>Wei, Pengcheng</creatorcontrib><creatorcontrib>Huang, Rongfeng</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</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>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>Qin, Hua</au><au>Zhang, Zhijin</au><au>Wang, Juan</au><au>Chen, Xinbing</au><au>Wei, Pengcheng</au><au>Huang, Rongfeng</au><au>Yu, Hao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The activation of OsEIL1 on YUC8 transcription and auxin biosynthesis is required for ethylene-inhibited root elongation in rice early seedling development</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2017-08</date><risdate>2017</risdate><volume>13</volume><issue>8</issue><spage>e1006955</spage><pages>e1006955-</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Rice is an important monocotyledonous crop worldwide; it differs from the dicotyledonous plant Arabidopsis in many aspects. In Arabidopsis, ethylene and auxin act synergistically to regulate root growth and development. However, their interaction in rice is still unclear. Here, we report that the transcriptional activation of OsEIL1 on the expression of YUC8/REIN7 and indole-3-pyruvic acid (IPA)-dependent auxin biosynthesis is required for ethylene-inhibited root elongation. Using an inhibitor of YUC activity, which regulates auxin biosynthesis via the conversion of IPA to indole-3-acetic acid (IAA), we showed that ethylene-inhibited primary root elongation is dependent on YUC-based auxin biosynthesis. By screening phenotypes of seedling primary root from mutagenesis libraries following ethylene treatment, we identified a rice ethylene-insensitive mutant, rein7-1, in which YUC8/REIN7 is truncated at its C-terminus. Mutation in YUC8/REIN7 reduced auxin biosynthesis in rice, while YUC8/REIN7 overexpression enhanced ethylene sensitivity in the roots. Moreover, YUC8/REIN7 catalyzed the conversion of IPA to IAA, truncated version at C-terminal end of the YUC8/REIN7 resulted in significant reduction of enzymatic activity, indicating that YUC8/REIN7 is required for IPA-dependent auxin biosynthesis and ethylene-inhibited root elongation in rice early seedlings. Further investigations indicated that ethylene induced YUC8/REIN7 expression and promoted auxin accumulation in roots. Addition of low concentrations of IAA rescued the ethylene response in the rein7-1, strongly demonstrating that ethylene-inhibited root elongation depends on IPA-dependent auxin biosynthesis. Genetic studies revealed that YUC8/REIN7-mediated auxin biosynthesis functioned downstream of OsEIL1, which directly activated the expression of YUC8/REIN7. Thus, our findings reveal a model of interaction between ethylene and auxin in rice seedling primary root elongation, enhancing our understanding of ethylene signaling in rice.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28829777</pmid><doi>10.1371/journal.pgen.1006955</doi><orcidid>https://orcid.org/0000-0001-9788-7290</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Acetic acid Arabidopsis Proteins - genetics Biology and Life Sciences Biosynthesis Biotechnology C-Terminus Elongation Enzymatic activity Ethylene Ethylenes - metabolism Funding Gene Expression Regulation, Plant Genes Indole-3-pyruvic acid Indoleacetic acid Indoleacetic Acids - metabolism Indoles - metabolism Low concentrations Mixed Function Oxygenases - genetics Mutagenesis Mutation Oryza - genetics Oryza - growth & development Physical Sciences Plant Development - genetics Plant Growth Regulators - genetics Plant Roots - genetics Plant Roots - growth & development Plants, Genetically Modified - genetics Pyruvic acid R&D Research & development Research and Analysis Methods Rice Roots Seedlings Seedlings - genetics Seedlings - growth & development Sensitivity enhancement Software Transcription activation Transcription Factors - genetics |
| title | The activation of OsEIL1 on YUC8 transcription and auxin biosynthesis is required for ethylene-inhibited root elongation in rice early seedling development |
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