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Functional bisporangiate cones in Pinus johannis (Pinaceae): Implications for the evolution of bisexuality in seed plants
Premise of study: Bisexuality (male and female function in one structure) has been reported as a key innovation of angiosperms. Although there are several reports of "teratological" bisporangiate (bisexual) cones in gymnosperms, there have been none on the viability of their ovules and pol...
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Published in: | American journal of botany 2011, Vol.98 (1), p.130-139 |
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container_title | American journal of botany |
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creator | Flores-Rentería, Lluvia Vázquez-Lobo, Alejandra Whipple, Amy V Piñero, Daniel Márquez-Guzmán, Judith Domínguez, C.A |
description | Premise of study: Bisexuality (male and female function in one structure) has been reported as a key innovation of angiosperms. Although there are several reports of "teratological" bisporangiate (bisexual) cones in gymnosperms, there have been none on the viability of their ovules and pollen. Analyses of the development and arrangement of female and male structures on bisporangiate cones of Pinus johannis enables us to gain insight on the origin of bisexuality in seed plants, for both angiosperms and gymnosperms. METHODS: Viability of bisporangiate cones was assayed by performing manual crosses and using anatomical and histological methods. Key results: We determined that bisporangiate cones of P. johannis produce functional pollen and ovules. Male and female organs occupy basal and apical positions, respectively, the same positions found in almost all bisporangiate strobili in gymnosperms and bisexual flowers in angiosperms. CONCLUSIONS: The viability and spatial distribution of female and male organs of bisporangiate cones and their frequent occurrence in gymnosperms suggest a common mechanism in all seed plants for the production of bisporangiate structures. This idea is further supported by the presence of homologous genes for sexual organ identity in gymnosperms and angiosperms as reported by other authors. The lack of bisporangiate structure in gymnosperms may be primarily due to selection to avoid inbreeding rather than to genetic constraint. |
doi_str_mv | 10.3732/ajb.1000275 |
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Although there are several reports of "teratological" bisporangiate (bisexual) cones in gymnosperms, there have been none on the viability of their ovules and pollen. Analyses of the development and arrangement of female and male structures on bisporangiate cones of Pinus johannis enables us to gain insight on the origin of bisexuality in seed plants, for both angiosperms and gymnosperms. METHODS: Viability of bisporangiate cones was assayed by performing manual crosses and using anatomical and histological methods. Key results: We determined that bisporangiate cones of P. johannis produce functional pollen and ovules. Male and female organs occupy basal and apical positions, respectively, the same positions found in almost all bisporangiate strobili in gymnosperms and bisexual flowers in angiosperms. CONCLUSIONS: The viability and spatial distribution of female and male organs of bisporangiate cones and their frequent occurrence in gymnosperms suggest a common mechanism in all seed plants for the production of bisporangiate structures. This idea is further supported by the presence of homologous genes for sexual organ identity in gymnosperms and angiosperms as reported by other authors. The lack of bisporangiate structure in gymnosperms may be primarily due to selection to avoid inbreeding rather than to genetic constraint.</description><identifier>ISSN: 0002-9122</identifier><identifier>EISSN: 1537-2197</identifier><identifier>DOI: 10.3732/ajb.1000275</identifier><identifier>PMID: 21613091</identifier><identifier>CODEN: AJBOAA</identifier><language>eng</language><publisher>United States: Botanical Society of America</publisher><subject><![CDATA[Angiosperms ; Bisexuality ; bisporangiate cones ; Botany ; breeding systems ; Cell Survival ; Conifers ; dioecy ; Evolution, Molecular ; Flowers ; Flowers - anatomy & histology ; Fruit - growth & development ; Genetics ; Gymnosperms ; Magnoliopsida - anatomy & histology ; Magnoliopsida - genetics ; Microsporocytes ; Molecular Sequence Data ; Ovule - growth & development ; Ovules ; Phylogeny ; Pinaceae ; Pinus - anatomy & histology ; Pinus - genetics ; Pinus - growth & development ; Pinus johannis ; Plant reproduction ; Plants ; Pollen ; Pollen - growth & development ; Reproductive Biology ; Seeds ; Seeds - growth & development ; Trees ; unisexuality ; Viability]]></subject><ispartof>American journal of botany, 2011, Vol.98 (1), p.130-139</ispartof><rights>Copyright 2011 Botanical Society of America, Inc.</rights><rights>2011 Botanical Society of America</rights><rights>Copyright Botanical Society of America, Inc. Jan 2011</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4030-bb5aa0805c33983f5754bb3dfb5493f75c9b72d1b8373f615733e62d5fa54e513</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/25766895$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/25766895$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,4024,27923,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21613091$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Flores-Rentería, Lluvia</creatorcontrib><creatorcontrib>Vázquez-Lobo, Alejandra</creatorcontrib><creatorcontrib>Whipple, Amy V</creatorcontrib><creatorcontrib>Piñero, Daniel</creatorcontrib><creatorcontrib>Márquez-Guzmán, Judith</creatorcontrib><creatorcontrib>Domínguez, C.A</creatorcontrib><title>Functional bisporangiate cones in Pinus johannis (Pinaceae): Implications for the evolution of bisexuality in seed plants</title><title>American journal of botany</title><addtitle>Am J Bot</addtitle><description>Premise of study: Bisexuality (male and female function in one structure) has been reported as a key innovation of angiosperms. Although there are several reports of "teratological" bisporangiate (bisexual) cones in gymnosperms, there have been none on the viability of their ovules and pollen. Analyses of the development and arrangement of female and male structures on bisporangiate cones of Pinus johannis enables us to gain insight on the origin of bisexuality in seed plants, for both angiosperms and gymnosperms. METHODS: Viability of bisporangiate cones was assayed by performing manual crosses and using anatomical and histological methods. Key results: We determined that bisporangiate cones of P. johannis produce functional pollen and ovules. Male and female organs occupy basal and apical positions, respectively, the same positions found in almost all bisporangiate strobili in gymnosperms and bisexual flowers in angiosperms. CONCLUSIONS: The viability and spatial distribution of female and male organs of bisporangiate cones and their frequent occurrence in gymnosperms suggest a common mechanism in all seed plants for the production of bisporangiate structures. This idea is further supported by the presence of homologous genes for sexual organ identity in gymnosperms and angiosperms as reported by other authors. The lack of bisporangiate structure in gymnosperms may be primarily due to selection to avoid inbreeding rather than to genetic constraint.</description><subject>Angiosperms</subject><subject>Bisexuality</subject><subject>bisporangiate cones</subject><subject>Botany</subject><subject>breeding systems</subject><subject>Cell Survival</subject><subject>Conifers</subject><subject>dioecy</subject><subject>Evolution, Molecular</subject><subject>Flowers</subject><subject>Flowers - anatomy & histology</subject><subject>Fruit - growth & development</subject><subject>Genetics</subject><subject>Gymnosperms</subject><subject>Magnoliopsida - anatomy & histology</subject><subject>Magnoliopsida - genetics</subject><subject>Microsporocytes</subject><subject>Molecular Sequence Data</subject><subject>Ovule - growth & development</subject><subject>Ovules</subject><subject>Phylogeny</subject><subject>Pinaceae</subject><subject>Pinus - anatomy & histology</subject><subject>Pinus - genetics</subject><subject>Pinus - growth & development</subject><subject>Pinus johannis</subject><subject>Plant reproduction</subject><subject>Plants</subject><subject>Pollen</subject><subject>Pollen - growth & development</subject><subject>Reproductive Biology</subject><subject>Seeds</subject><subject>Seeds - growth & development</subject><subject>Trees</subject><subject>unisexuality</subject><subject>Viability</subject><issn>0002-9122</issn><issn>1537-2197</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNp9kc1vFSEUxYnR2OfTlWuVuFFjpvIxDIO72litaaKJdk2AgZbJPBhhpvX99zLOUxMXrsi9_M65cA8AjzE6ppySN6rXxxghRDi7AzaYUV4RLPhdsFmalcCEHIEHOfelFLUg98ERwQ2mSOAN2J_NwUw-BjVA7fMYkwpXXk0Wmhhshj7ALz7MGfbxWoXgM3xZamWssq_ewvPdOHijFn2GLiY4XVtob-IwLy0Y3eJpf8xq8NN-8crWdnAcVJjyQ3DPqSHbR4dzCy7P3n87_VhdfP5wfnpyUZkaUVRpzZRCLWKGUtFSxzirtaad06wW1HFmhOakw7oty3ANZpxS25COOcVqyzDdgher75ji99nmSe58NnYoj7BxzrJtWiEYKWZb8Pwfso9zKpspECGMoZY3BXq9QibFnJN1ckx-p9JeYiSXPGTJQx7yKPTTg-Wsd7b7w_4OoAB4BW79YPf_85Inn94RVFRF82TV9HmK6a8n4035yzL02XrvVJTqKvksL7_-kmJBCS0b-gnXr6e2</recordid><startdate>2011</startdate><enddate>2011</enddate><creator>Flores-Rentería, Lluvia</creator><creator>Vázquez-Lobo, Alejandra</creator><creator>Whipple, Amy V</creator><creator>Piñero, Daniel</creator><creator>Márquez-Guzmán, Judith</creator><creator>Domínguez, C.A</creator><general>Botanical Society of America</general><general>Botanical Society of America, Inc</general><scope>FBQ</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>7QL</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope></search><sort><creationdate>2011</creationdate><title>Functional bisporangiate cones in Pinus johannis (Pinaceae): Implications for the evolution of bisexuality in seed plants</title><author>Flores-Rentería, Lluvia ; Vázquez-Lobo, Alejandra ; Whipple, Amy V ; Piñero, Daniel ; Márquez-Guzmán, Judith ; Domínguez, C.A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4030-bb5aa0805c33983f5754bb3dfb5493f75c9b72d1b8373f615733e62d5fa54e513</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Angiosperms</topic><topic>Bisexuality</topic><topic>bisporangiate cones</topic><topic>Botany</topic><topic>breeding systems</topic><topic>Cell Survival</topic><topic>Conifers</topic><topic>dioecy</topic><topic>Evolution, Molecular</topic><topic>Flowers</topic><topic>Flowers - anatomy & histology</topic><topic>Fruit - growth & development</topic><topic>Genetics</topic><topic>Gymnosperms</topic><topic>Magnoliopsida - anatomy & histology</topic><topic>Magnoliopsida - genetics</topic><topic>Microsporocytes</topic><topic>Molecular Sequence Data</topic><topic>Ovule - growth & development</topic><topic>Ovules</topic><topic>Phylogeny</topic><topic>Pinaceae</topic><topic>Pinus - anatomy & histology</topic><topic>Pinus - genetics</topic><topic>Pinus - growth & development</topic><topic>Pinus johannis</topic><topic>Plant reproduction</topic><topic>Plants</topic><topic>Pollen</topic><topic>Pollen - growth & development</topic><topic>Reproductive Biology</topic><topic>Seeds</topic><topic>Seeds - growth & development</topic><topic>Trees</topic><topic>unisexuality</topic><topic>Viability</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Flores-Rentería, Lluvia</creatorcontrib><creatorcontrib>Vázquez-Lobo, Alejandra</creatorcontrib><creatorcontrib>Whipple, Amy V</creatorcontrib><creatorcontrib>Piñero, Daniel</creatorcontrib><creatorcontrib>Márquez-Guzmán, Judith</creatorcontrib><creatorcontrib>Domínguez, C.A</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>American journal of botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Flores-Rentería, Lluvia</au><au>Vázquez-Lobo, Alejandra</au><au>Whipple, Amy V</au><au>Piñero, Daniel</au><au>Márquez-Guzmán, Judith</au><au>Domínguez, C.A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional bisporangiate cones in Pinus johannis (Pinaceae): Implications for the evolution of bisexuality in seed plants</atitle><jtitle>American journal of botany</jtitle><addtitle>Am J Bot</addtitle><date>2011</date><risdate>2011</risdate><volume>98</volume><issue>1</issue><spage>130</spage><epage>139</epage><pages>130-139</pages><issn>0002-9122</issn><eissn>1537-2197</eissn><coden>AJBOAA</coden><abstract>Premise of study: Bisexuality (male and female function in one structure) has been reported as a key innovation of angiosperms. Although there are several reports of "teratological" bisporangiate (bisexual) cones in gymnosperms, there have been none on the viability of their ovules and pollen. Analyses of the development and arrangement of female and male structures on bisporangiate cones of Pinus johannis enables us to gain insight on the origin of bisexuality in seed plants, for both angiosperms and gymnosperms. METHODS: Viability of bisporangiate cones was assayed by performing manual crosses and using anatomical and histological methods. Key results: We determined that bisporangiate cones of P. johannis produce functional pollen and ovules. Male and female organs occupy basal and apical positions, respectively, the same positions found in almost all bisporangiate strobili in gymnosperms and bisexual flowers in angiosperms. CONCLUSIONS: The viability and spatial distribution of female and male organs of bisporangiate cones and their frequent occurrence in gymnosperms suggest a common mechanism in all seed plants for the production of bisporangiate structures. This idea is further supported by the presence of homologous genes for sexual organ identity in gymnosperms and angiosperms as reported by other authors. The lack of bisporangiate structure in gymnosperms may be primarily due to selection to avoid inbreeding rather than to genetic constraint.</abstract><cop>United States</cop><pub>Botanical Society of America</pub><pmid>21613091</pmid><doi>10.3732/ajb.1000275</doi><tpages>10</tpages></addata></record> |
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subjects | Angiosperms Bisexuality bisporangiate cones Botany breeding systems Cell Survival Conifers dioecy Evolution, Molecular Flowers Flowers - anatomy & histology Fruit - growth & development Genetics Gymnosperms Magnoliopsida - anatomy & histology Magnoliopsida - genetics Microsporocytes Molecular Sequence Data Ovule - growth & development Ovules Phylogeny Pinaceae Pinus - anatomy & histology Pinus - genetics Pinus - growth & development Pinus johannis Plant reproduction Plants Pollen Pollen - growth & development Reproductive Biology Seeds Seeds - growth & development Trees unisexuality Viability |
title | Functional bisporangiate cones in Pinus johannis (Pinaceae): Implications for the evolution of bisexuality in seed plants |
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