RNA interference suppression of AGAMOUS and SEEDSTICK alters floral organ identity and impairs floral organ determinacy, ovule differentiation, and seed-hair development in Populus
The role of the floral homeotic gene AGAMOUS (AG) and its close homologues in development of anemophilous, unisexual catkins has not previously been studied. We transformed two RNA interference (RNAi) constructs, PTG and its matrix-attachmentregion flanked version MPG, into the early-flowering femal...
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| Veröffentlicht in: | The New phytologist 2019-04, Vol.222 (2), p.923-937 |
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| creator | Lu, Haiwei Klocko, Amy L. Brunner, Amy M. Ma, Cathleen Magnuson, Anna C. Howe, Glenn T. An, Xinmin Strauss, Steven H. |
| description | The role of the floral homeotic gene AGAMOUS (AG) and its close homologues in development of anemophilous, unisexual catkins has not previously been studied.
We transformed two RNA interference (RNAi) constructs, PTG and its matrix-attachmentregion flanked version MPG, into the early-flowering female poplar clone 6K10 (Populus alba) to suppress the expression of its two duplicate AG orthologues.
By early 2018, six out of 22 flowering PTG events and 11 out of 12 flowering MPG events showed modified floral phenotypes in a field trial in Oregon, USA. Flowers in catkins from modified events had ‘carpel-inside-carpel’ phenotypes. Complete disruption of seed production was observed in seven events, and sterile anther-like organs in 10 events. Events with strong co-suppression of both the two AG and two SEEDSTICK (STK) paralogues lacked both seeds and associated seed hairs. Alterations in all of the modified floral phenotypes were stable over 4 yr of study. Trees from floral-modified events did not differ significantly (P < 0.05) from nonmodified transgenic or nontransgenic controls in biomass growth or leaf morphology.
AG and STK genes show strong conservation of gene function during poplar catkin development and are promising targets for genetic containment of exotic or genetically engineered trees. |
| doi_str_mv | 10.1111/nph.15648 |
| format | Article |
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We transformed two RNA interference (RNAi) constructs, PTG and its matrix-attachmentregion flanked version MPG, into the early-flowering female poplar clone 6K10 (Populus alba) to suppress the expression of its two duplicate AG orthologues.
By early 2018, six out of 22 flowering PTG events and 11 out of 12 flowering MPG events showed modified floral phenotypes in a field trial in Oregon, USA. Flowers in catkins from modified events had ‘carpel-inside-carpel’ phenotypes. Complete disruption of seed production was observed in seven events, and sterile anther-like organs in 10 events. Events with strong co-suppression of both the two AG and two SEEDSTICK (STK) paralogues lacked both seeds and associated seed hairs. Alterations in all of the modified floral phenotypes were stable over 4 yr of study. Trees from floral-modified events did not differ significantly (P < 0.05) from nonmodified transgenic or nontransgenic controls in biomass growth or leaf morphology.
AG and STK genes show strong conservation of gene function during poplar catkin development and are promising targets for genetic containment of exotic or genetically engineered trees.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.15648</identifier><identifier>PMID: 30565259</identifier><language>eng</language><publisher>England: Wiley</publisher><subject><![CDATA[AGAMOUS ; biomass ; Body organs ; catkins ; Containment ; females ; field experimentation ; Flowering ; Flowers ; Flowers - anatomy & histology ; Gene expression ; Gene Expression Regulation, Plant ; Genetic engineering ; homeotic genes ; Homology ; Interference ; leaf morphology ; matrix attachment region ; Morphology ; Oregon ; Organs ; ovules ; phenotype ; Phenotypes ; Plant Leaves - anatomy & histology ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants, Genetically Modified ; Poplar ; Populus ; Populus - anatomy & histology ; Populus - genetics ; Populus - growth & development ; Populus - metabolism ; Populus alba ; Ribonucleic acid ; RNA ; RNA Interference ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; RNA-mediated interference ; RNAi ; Seed production ; Seeds ; Seeds - anatomy & histology ; SEEDSTICK ; sterility ; transgenic plants ; Trees ; Trees - growth & development]]></subject><ispartof>The New phytologist, 2019-04, Vol.222 (2), p.923-937</ispartof><rights>2018 The Authors © 2018 New Phytologist Trust</rights><rights>2018 The Authors. New Phytologist © 2018 New Phytologist Trust</rights><rights>2018 The Authors. New Phytologist © 2018 New Phytologist Trust.</rights><rights>2018. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4988-170ddea75a07445c8ad43ccd7f02c330a92919d65124e10a3939a7671c8be4f53</citedby><cites>FETCH-LOGICAL-c4988-170ddea75a07445c8ad43ccd7f02c330a92919d65124e10a3939a7671c8be4f53</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26629301$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26629301$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,1411,1427,27903,27904,45553,45554,46387,46811,57995,58228</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30565259$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lu, Haiwei</creatorcontrib><creatorcontrib>Klocko, Amy L.</creatorcontrib><creatorcontrib>Brunner, Amy M.</creatorcontrib><creatorcontrib>Ma, Cathleen</creatorcontrib><creatorcontrib>Magnuson, Anna C.</creatorcontrib><creatorcontrib>Howe, Glenn T.</creatorcontrib><creatorcontrib>An, Xinmin</creatorcontrib><creatorcontrib>Strauss, Steven H.</creatorcontrib><title>RNA interference suppression of AGAMOUS and SEEDSTICK alters floral organ identity and impairs floral organ determinacy, ovule differentiation, and seed-hair development in Populus</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>The role of the floral homeotic gene AGAMOUS (AG) and its close homologues in development of anemophilous, unisexual catkins has not previously been studied.
We transformed two RNA interference (RNAi) constructs, PTG and its matrix-attachmentregion flanked version MPG, into the early-flowering female poplar clone 6K10 (Populus alba) to suppress the expression of its two duplicate AG orthologues.
By early 2018, six out of 22 flowering PTG events and 11 out of 12 flowering MPG events showed modified floral phenotypes in a field trial in Oregon, USA. Flowers in catkins from modified events had ‘carpel-inside-carpel’ phenotypes. Complete disruption of seed production was observed in seven events, and sterile anther-like organs in 10 events. Events with strong co-suppression of both the two AG and two SEEDSTICK (STK) paralogues lacked both seeds and associated seed hairs. Alterations in all of the modified floral phenotypes were stable over 4 yr of study. Trees from floral-modified events did not differ significantly (P < 0.05) from nonmodified transgenic or nontransgenic controls in biomass growth or leaf morphology.
AG and STK genes show strong conservation of gene function during poplar catkin development and are promising targets for genetic containment of exotic or genetically engineered trees.</description><subject>AGAMOUS</subject><subject>biomass</subject><subject>Body organs</subject><subject>catkins</subject><subject>Containment</subject><subject>females</subject><subject>field experimentation</subject><subject>Flowering</subject><subject>Flowers</subject><subject>Flowers - anatomy & histology</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genetic engineering</subject><subject>homeotic genes</subject><subject>Homology</subject><subject>Interference</subject><subject>leaf morphology</subject><subject>matrix attachment region</subject><subject>Morphology</subject><subject>Oregon</subject><subject>Organs</subject><subject>ovules</subject><subject>phenotype</subject><subject>Phenotypes</subject><subject>Plant Leaves - anatomy & histology</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants, Genetically Modified</subject><subject>Poplar</subject><subject>Populus</subject><subject>Populus - anatomy & histology</subject><subject>Populus - genetics</subject><subject>Populus - growth & development</subject><subject>Populus - metabolism</subject><subject>Populus alba</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA Interference</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>RNA-mediated interference</subject><subject>RNAi</subject><subject>Seed production</subject><subject>Seeds</subject><subject>Seeds - anatomy & histology</subject><subject>SEEDSTICK</subject><subject>sterility</subject><subject>transgenic plants</subject><subject>Trees</subject><subject>Trees - growth & development</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNqFkt9u0zAYxS0EYl3hggcAWeIGpGWzndiJb5CqrmwTY5voJnFnebazukrsYCdFfS8eEK_dKpiE8M134d853x8dAN5gdIjTO3Ld4hBTVlTPwAgXjGcVzsvnYIQQqTJWsO97YD_GJUKIU0Zegr0cUUYJ5SPw69vFBFrXm1CbYJwyMA5dF0yM1jvoazg5mXy9vJlD6TScz2bH8-uz6Rcom6SIsG58kA304U46aLVxve3XG9S2nbRPCW2SqrVOqvUB9KuhMVDbetO4t7JPHQ824miMzhZJnxQr0_iuTUCaEl75bmiG-Aq8qGUTzeuHOgY3n2fX09Ps_PLkbDo5z1TBqyrDJdLayJJKVBYFVZXURa6ULmtEVJ4jyQnHXDOKSWEwkjnPuSxZiVV1a4qa5mPwaevbDbet0SpNkZYRXbCtDGvhpRV__zi7EHd-JRjlCCe7MfjwYBD8j8HEXrQ2KtM00hk_REFyTEnFSlT-H8W0opRjcu_6_gm69ENw6RKCUMxZgQrEEvVxS6ngYwym3s2NkbiPjUixEZvYJPbdn4vuyMecJOBoC_y0jVn_20lcXJ0-Wr7dKpax92GnIIylDdJxfgOLbNha</recordid><startdate>201904</startdate><enddate>201904</enddate><creator>Lu, Haiwei</creator><creator>Klocko, Amy L.</creator><creator>Brunner, Amy M.</creator><creator>Ma, Cathleen</creator><creator>Magnuson, Anna C.</creator><creator>Howe, Glenn T.</creator><creator>An, Xinmin</creator><creator>Strauss, Steven H.</creator><general>Wiley</general><general>Wiley Subscription Services, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><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>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>201904</creationdate><title>RNA interference suppression of AGAMOUS and SEEDSTICK alters floral organ identity and impairs floral organ determinacy, ovule differentiation, and seed-hair development in Populus</title><author>Lu, Haiwei ; Klocko, Amy L. ; Brunner, Amy M. ; Ma, Cathleen ; Magnuson, Anna C. ; Howe, Glenn T. ; An, Xinmin ; Strauss, Steven H.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4988-170ddea75a07445c8ad43ccd7f02c330a92919d65124e10a3939a7671c8be4f53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>AGAMOUS</topic><topic>biomass</topic><topic>Body organs</topic><topic>catkins</topic><topic>Containment</topic><topic>females</topic><topic>field experimentation</topic><topic>Flowering</topic><topic>Flowers</topic><topic>Flowers - anatomy & histology</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genetic engineering</topic><topic>homeotic genes</topic><topic>Homology</topic><topic>Interference</topic><topic>leaf morphology</topic><topic>matrix attachment region</topic><topic>Morphology</topic><topic>Oregon</topic><topic>Organs</topic><topic>ovules</topic><topic>phenotype</topic><topic>Phenotypes</topic><topic>Plant Leaves - anatomy & histology</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants, Genetically Modified</topic><topic>Poplar</topic><topic>Populus</topic><topic>Populus - anatomy & histology</topic><topic>Populus - genetics</topic><topic>Populus - growth & development</topic><topic>Populus - metabolism</topic><topic>Populus alba</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA Interference</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>RNA-mediated interference</topic><topic>RNAi</topic><topic>Seed production</topic><topic>Seeds</topic><topic>Seeds - anatomy & histology</topic><topic>SEEDSTICK</topic><topic>sterility</topic><topic>transgenic plants</topic><topic>Trees</topic><topic>Trees - growth & development</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lu, Haiwei</creatorcontrib><creatorcontrib>Klocko, Amy L.</creatorcontrib><creatorcontrib>Brunner, Amy M.</creatorcontrib><creatorcontrib>Ma, Cathleen</creatorcontrib><creatorcontrib>Magnuson, Anna C.</creatorcontrib><creatorcontrib>Howe, Glenn T.</creatorcontrib><creatorcontrib>An, Xinmin</creatorcontrib><creatorcontrib>Strauss, Steven H.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lu, Haiwei</au><au>Klocko, Amy L.</au><au>Brunner, Amy M.</au><au>Ma, Cathleen</au><au>Magnuson, Anna C.</au><au>Howe, Glenn T.</au><au>An, Xinmin</au><au>Strauss, Steven H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>RNA interference suppression of AGAMOUS and SEEDSTICK alters floral organ identity and impairs floral organ determinacy, ovule differentiation, and seed-hair development in Populus</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2019-04</date><risdate>2019</risdate><volume>222</volume><issue>2</issue><spage>923</spage><epage>937</epage><pages>923-937</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>The role of the floral homeotic gene AGAMOUS (AG) and its close homologues in development of anemophilous, unisexual catkins has not previously been studied.
We transformed two RNA interference (RNAi) constructs, PTG and its matrix-attachmentregion flanked version MPG, into the early-flowering female poplar clone 6K10 (Populus alba) to suppress the expression of its two duplicate AG orthologues.
By early 2018, six out of 22 flowering PTG events and 11 out of 12 flowering MPG events showed modified floral phenotypes in a field trial in Oregon, USA. Flowers in catkins from modified events had ‘carpel-inside-carpel’ phenotypes. Complete disruption of seed production was observed in seven events, and sterile anther-like organs in 10 events. Events with strong co-suppression of both the two AG and two SEEDSTICK (STK) paralogues lacked both seeds and associated seed hairs. Alterations in all of the modified floral phenotypes were stable over 4 yr of study. Trees from floral-modified events did not differ significantly (P < 0.05) from nonmodified transgenic or nontransgenic controls in biomass growth or leaf morphology.
AG and STK genes show strong conservation of gene function during poplar catkin development and are promising targets for genetic containment of exotic or genetically engineered trees.</abstract><cop>England</cop><pub>Wiley</pub><pmid>30565259</pmid><doi>10.1111/nph.15648</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | AGAMOUS biomass Body organs catkins Containment females field experimentation Flowering Flowers Flowers - anatomy & histology Gene expression Gene Expression Regulation, Plant Genetic engineering homeotic genes Homology Interference leaf morphology matrix attachment region Morphology Oregon Organs ovules phenotype Phenotypes Plant Leaves - anatomy & histology Plant Proteins - genetics Plant Proteins - metabolism Plants, Genetically Modified Poplar Populus Populus - anatomy & histology Populus - genetics Populus - growth & development Populus - metabolism Populus alba Ribonucleic acid RNA RNA Interference RNA, Messenger - genetics RNA, Messenger - metabolism RNA-mediated interference RNAi Seed production Seeds Seeds - anatomy & histology SEEDSTICK sterility transgenic plants Trees Trees - growth & development |
| title | RNA interference suppression of AGAMOUS and SEEDSTICK alters floral organ identity and impairs floral organ determinacy, ovule differentiation, and seed-hair development in Populus |
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