The MicroRNA390/TAS3 Pathway Mediates Symbiotic Nodulation and Lateral Root Growth
Legume roots form two types of postembryonic organs, lateral roots and symbiotic nodules. Nodule formation is the result of the interaction of legumes with rhizobia and requires the mitotic activation and differentiation of root cells as well as an independent, but coordinated, program that allows i...
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| Veröffentlicht in: | Plant physiology (Bethesda) 2017-08, Vol.174 (4), p.2469-2486 |
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| creator | Hobecker, Karen Vanesa Reynoso, Mauricio Alberto Bustos-Sanmamed, Pilar Wen, Jiangqi Mysore, Kirankumar S. Crespi, Martín Blanco, Flavio Antonio Zanetti, María Eugenia |
| description | Legume roots form two types of postembryonic organs, lateral roots and symbiotic nodules. Nodule formation is the result of the interaction of legumes with rhizobia and requires the mitotic activation and differentiation of root cells as well as an independent, but coordinated, program that allows infection by rhizobia. MicroRNA390 (miR390) is an evolutionarily conserved microRNA that targets the Trans-Acting Short Interference RNA3 (TAS3) transcript. Cleavage of TAS3 by ARGONAUTE7 results in the production of trans-acting small interference RNAs, which target mRNAs encoding AUXIN RESPONSE FACTOR2 (ARF2), ARF3, and ARF4. Here, we show that activation of the miR390/TAS3 regulatory module by overexpression of miR390 in Medicago truncatula promotes lateral root growth but prevents nodule organogenesis, rhizobial infection, and the induction of two key nodulation genes, Nodulation Signaling Pathway1 (NSP1) and NSP2. Accordingly, inactivation of the miR390/TAS3 module, either by expression of a miR390 target mimicry construct or mutations in ARGONAUTE7, enhances nodulation and rhizobial infection, alters the spatial distribution of the nodules, and increases the percentage of nodules with multiple meristems. Our results revealed a key role of the miR390/TAS3 pathway in legumes as a modulator of lateral root organs, playing opposite roles in lateral root and nodule development. |
| doi_str_mv | 10.1104/pp.17.00464 |
| format | Article |
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Nodule formation is the result of the interaction of legumes with rhizobia and requires the mitotic activation and differentiation of root cells as well as an independent, but coordinated, program that allows infection by rhizobia. MicroRNA390 (miR390) is an evolutionarily conserved microRNA that targets the Trans-Acting Short Interference RNA3 (TAS3) transcript. Cleavage of TAS3 by ARGONAUTE7 results in the production of trans-acting small interference RNAs, which target mRNAs encoding AUXIN RESPONSE FACTOR2 (ARF2), ARF3, and ARF4. Here, we show that activation of the miR390/TAS3 regulatory module by overexpression of miR390 in Medicago truncatula promotes lateral root growth but prevents nodule organogenesis, rhizobial infection, and the induction of two key nodulation genes, Nodulation Signaling Pathway1 (NSP1) and NSP2. Accordingly, inactivation of the miR390/TAS3 module, either by expression of a miR390 target mimicry construct or mutations in ARGONAUTE7, enhances nodulation and rhizobial infection, alters the spatial distribution of the nodules, and increases the percentage of nodules with multiple meristems. Our results revealed a key role of the miR390/TAS3 pathway in legumes as a modulator of lateral root organs, playing opposite roles in lateral root and nodule development.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.17.00464</identifier><identifier>PMID: 28663332</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Gene Expression Regulation, Developmental ; Gene Expression Regulation, Plant ; Life Sciences ; Medicago truncatula - genetics ; Medicago truncatula - growth & development ; Medicago truncatula - microbiology ; MicroRNAs - genetics ; MicroRNAs - metabolism ; Models, Biological ; Mutation - genetics ; Organ Specificity - genetics ; Plant Proteins - metabolism ; Plant Root Nodulation - genetics ; Plant Roots - genetics ; Plant Roots - growth & development ; Plant Roots - microbiology ; Plant Roots - ultrastructure ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Root Nodules, Plant - metabolism ; Root Nodules, Plant - microbiology ; Root Nodules, Plant - ultrastructure ; SIGNALING AND RESPONSE ; Sinorhizobium meliloti - physiology ; Symbiosis - genetics ; Vegetal Biology</subject><ispartof>Plant physiology (Bethesda), 2017-08, Vol.174 (4), p.2469-2486</ispartof><rights>2017 American Society of Plant Biologists</rights><rights>2017 American Society of Plant Biologists. All Rights Reserved.</rights><rights>Copyright</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c382t-606c6ae13ccccac559f32bb2681de1258c61d4ea34451ac4c9242ad31c196a293</citedby><orcidid>0000-0001-5113-7750 ; 0000-0001-9565-1743 ; 0000-0002-9990-5808 ; 0000-0002-5052-289X ; 0000-0002-5698-9482 ; 0000-0002-8380-8472</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26375266$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26375266$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,803,885,27924,27925,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28663332$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02629133$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Hobecker, Karen Vanesa</creatorcontrib><creatorcontrib>Reynoso, Mauricio Alberto</creatorcontrib><creatorcontrib>Bustos-Sanmamed, Pilar</creatorcontrib><creatorcontrib>Wen, Jiangqi</creatorcontrib><creatorcontrib>Mysore, Kirankumar S.</creatorcontrib><creatorcontrib>Crespi, Martín</creatorcontrib><creatorcontrib>Blanco, Flavio Antonio</creatorcontrib><creatorcontrib>Zanetti, María Eugenia</creatorcontrib><title>The MicroRNA390/TAS3 Pathway Mediates Symbiotic Nodulation and Lateral Root Growth</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Legume roots form two types of postembryonic organs, lateral roots and symbiotic nodules. Nodule formation is the result of the interaction of legumes with rhizobia and requires the mitotic activation and differentiation of root cells as well as an independent, but coordinated, program that allows infection by rhizobia. MicroRNA390 (miR390) is an evolutionarily conserved microRNA that targets the Trans-Acting Short Interference RNA3 (TAS3) transcript. Cleavage of TAS3 by ARGONAUTE7 results in the production of trans-acting small interference RNAs, which target mRNAs encoding AUXIN RESPONSE FACTOR2 (ARF2), ARF3, and ARF4. Here, we show that activation of the miR390/TAS3 regulatory module by overexpression of miR390 in Medicago truncatula promotes lateral root growth but prevents nodule organogenesis, rhizobial infection, and the induction of two key nodulation genes, Nodulation Signaling Pathway1 (NSP1) and NSP2. Accordingly, inactivation of the miR390/TAS3 module, either by expression of a miR390 target mimicry construct or mutations in ARGONAUTE7, enhances nodulation and rhizobial infection, alters the spatial distribution of the nodules, and increases the percentage of nodules with multiple meristems. Our results revealed a key role of the miR390/TAS3 pathway in legumes as a modulator of lateral root organs, playing opposite roles in lateral root and nodule development.</description><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Expression Regulation, Plant</subject><subject>Life Sciences</subject><subject>Medicago truncatula - genetics</subject><subject>Medicago truncatula - growth & development</subject><subject>Medicago truncatula - microbiology</subject><subject>MicroRNAs - genetics</subject><subject>MicroRNAs - metabolism</subject><subject>Models, Biological</subject><subject>Mutation - genetics</subject><subject>Organ Specificity - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Root Nodulation - genetics</subject><subject>Plant Roots - genetics</subject><subject>Plant Roots - growth & development</subject><subject>Plant Roots - microbiology</subject><subject>Plant Roots - ultrastructure</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Root Nodules, Plant - metabolism</subject><subject>Root Nodules, Plant - microbiology</subject><subject>Root Nodules, Plant - ultrastructure</subject><subject>SIGNALING AND RESPONSE</subject><subject>Sinorhizobium meliloti - physiology</subject><subject>Symbiosis - genetics</subject><subject>Vegetal Biology</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpFkE1PAjEQhhujEURPnjU9agzQabvd3SMxfiWgBvDcDN0S1ix03RYN_94iinOZybxP3sNDyDmwHgCT_bruQdpjTCp5QNqQCN7licwOSZuxeLMsy1vkxPt3xhgIkMekxTOlhBC8TcbThaWj0jRu_DwQOetPBxNBXzEsvnBDR7YoMVhPJ5vlrHShNPTZFesKQ-lWFFcFHca4wYqOnQv0oXFfYXFKjuZYeXv2uzvk7f5uevvYHb48PN0Ohl0jMh66iimj0IIwcdAkST4XfDbjKoPCAk8yo6CQFoWUCaCRJueSYyHAQK6Q56JDrne9C6x03ZRLbDbaYakfB0O9_TGueA5CfEJkr3Zs3biPtfVBL0tvbFXhyrq115BHb1Kl6Ra92aHRifeNne-7gemtcF3XGlL9IzzSl7_F69nSFnv2z3AELnbAuw-u-c-VSBMemW-NX4Ip</recordid><startdate>20170801</startdate><enddate>20170801</enddate><creator>Hobecker, Karen Vanesa</creator><creator>Reynoso, Mauricio Alberto</creator><creator>Bustos-Sanmamed, Pilar</creator><creator>Wen, Jiangqi</creator><creator>Mysore, Kirankumar S.</creator><creator>Crespi, Martín</creator><creator>Blanco, Flavio Antonio</creator><creator>Zanetti, María Eugenia</creator><general>American Society of Plant Biologists</general><general>Oxford University Press ; 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>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0001-5113-7750</orcidid><orcidid>https://orcid.org/0000-0001-9565-1743</orcidid><orcidid>https://orcid.org/0000-0002-9990-5808</orcidid><orcidid>https://orcid.org/0000-0002-5052-289X</orcidid><orcidid>https://orcid.org/0000-0002-5698-9482</orcidid><orcidid>https://orcid.org/0000-0002-8380-8472</orcidid></search><sort><creationdate>20170801</creationdate><title>The MicroRNA390/TAS3 Pathway Mediates Symbiotic Nodulation and Lateral Root Growth</title><author>Hobecker, Karen Vanesa ; Reynoso, Mauricio Alberto ; Bustos-Sanmamed, Pilar ; Wen, Jiangqi ; Mysore, Kirankumar S. ; Crespi, Martín ; Blanco, Flavio Antonio ; Zanetti, María Eugenia</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c382t-606c6ae13ccccac559f32bb2681de1258c61d4ea34451ac4c9242ad31c196a293</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Gene Expression Regulation, Developmental</topic><topic>Gene Expression Regulation, Plant</topic><topic>Life Sciences</topic><topic>Medicago truncatula - genetics</topic><topic>Medicago truncatula - growth & development</topic><topic>Medicago truncatula - microbiology</topic><topic>MicroRNAs - genetics</topic><topic>MicroRNAs - metabolism</topic><topic>Models, Biological</topic><topic>Mutation - genetics</topic><topic>Organ Specificity - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Root Nodulation - genetics</topic><topic>Plant Roots - genetics</topic><topic>Plant Roots - growth & development</topic><topic>Plant Roots - microbiology</topic><topic>Plant Roots - ultrastructure</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Root Nodules, Plant - metabolism</topic><topic>Root Nodules, Plant - microbiology</topic><topic>Root Nodules, Plant - ultrastructure</topic><topic>SIGNALING AND RESPONSE</topic><topic>Sinorhizobium meliloti - physiology</topic><topic>Symbiosis - genetics</topic><topic>Vegetal Biology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hobecker, Karen Vanesa</creatorcontrib><creatorcontrib>Reynoso, Mauricio Alberto</creatorcontrib><creatorcontrib>Bustos-Sanmamed, Pilar</creatorcontrib><creatorcontrib>Wen, Jiangqi</creatorcontrib><creatorcontrib>Mysore, Kirankumar S.</creatorcontrib><creatorcontrib>Crespi, Martín</creatorcontrib><creatorcontrib>Blanco, Flavio Antonio</creatorcontrib><creatorcontrib>Zanetti, María Eugenia</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hobecker, Karen Vanesa</au><au>Reynoso, Mauricio Alberto</au><au>Bustos-Sanmamed, Pilar</au><au>Wen, Jiangqi</au><au>Mysore, Kirankumar S.</au><au>Crespi, Martín</au><au>Blanco, Flavio Antonio</au><au>Zanetti, María Eugenia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The MicroRNA390/TAS3 Pathway Mediates Symbiotic Nodulation and Lateral Root Growth</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2017-08-01</date><risdate>2017</risdate><volume>174</volume><issue>4</issue><spage>2469</spage><epage>2486</epage><pages>2469-2486</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><abstract>Legume roots form two types of postembryonic organs, lateral roots and symbiotic nodules. Nodule formation is the result of the interaction of legumes with rhizobia and requires the mitotic activation and differentiation of root cells as well as an independent, but coordinated, program that allows infection by rhizobia. MicroRNA390 (miR390) is an evolutionarily conserved microRNA that targets the Trans-Acting Short Interference RNA3 (TAS3) transcript. Cleavage of TAS3 by ARGONAUTE7 results in the production of trans-acting small interference RNAs, which target mRNAs encoding AUXIN RESPONSE FACTOR2 (ARF2), ARF3, and ARF4. Here, we show that activation of the miR390/TAS3 regulatory module by overexpression of miR390 in Medicago truncatula promotes lateral root growth but prevents nodule organogenesis, rhizobial infection, and the induction of two key nodulation genes, Nodulation Signaling Pathway1 (NSP1) and NSP2. Accordingly, inactivation of the miR390/TAS3 module, either by expression of a miR390 target mimicry construct or mutations in ARGONAUTE7, enhances nodulation and rhizobial infection, alters the spatial distribution of the nodules, and increases the percentage of nodules with multiple meristems. Our results revealed a key role of the miR390/TAS3 pathway in legumes as a modulator of lateral root organs, playing opposite roles in lateral root and nodule development.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>28663332</pmid><doi>10.1104/pp.17.00464</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0001-5113-7750</orcidid><orcidid>https://orcid.org/0000-0001-9565-1743</orcidid><orcidid>https://orcid.org/0000-0002-9990-5808</orcidid><orcidid>https://orcid.org/0000-0002-5052-289X</orcidid><orcidid>https://orcid.org/0000-0002-5698-9482</orcidid><orcidid>https://orcid.org/0000-0002-8380-8472</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; JSTOR Archive Collection A-Z Listing; Oxford University Press Journals All Titles (1996-Current) |
| subjects | Gene Expression Regulation, Developmental Gene Expression Regulation, Plant Life Sciences Medicago truncatula - genetics Medicago truncatula - growth & development Medicago truncatula - microbiology MicroRNAs - genetics MicroRNAs - metabolism Models, Biological Mutation - genetics Organ Specificity - genetics Plant Proteins - metabolism Plant Root Nodulation - genetics Plant Roots - genetics Plant Roots - growth & development Plant Roots - microbiology Plant Roots - ultrastructure RNA, Messenger - genetics RNA, Messenger - metabolism Root Nodules, Plant - metabolism Root Nodules, Plant - microbiology Root Nodules, Plant - ultrastructure SIGNALING AND RESPONSE Sinorhizobium meliloti - physiology Symbiosis - genetics Vegetal Biology |
| title | The MicroRNA390/TAS3 Pathway Mediates Symbiotic Nodulation and Lateral Root Growth |
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