A Cascade of Sequentially Expressed Sucrose Transporters in the Seed Coat and Endosperm Provides Nutrition for the Arabidopsis Embryo
Developing plant embryos depend on nutrition from maternal tissues via the seed coat and endosperm, but the mechanisms that supply nutrients to plant embryos have remained elusive. Sucrose, the major transport form of carbohydrate in plants, is delivered via the phloem to the maternal seed coat and...
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| Veröffentlicht in: | The Plant cell 2015-03, Vol.27 (3), p.607-619 |
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| container_title | The Plant cell |
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| creator | Chen, Li-Qing Lin, I Winnie Qu, Xiao-Qing Sosso, Davide McFarlane, Heather E. Londoño, Alejandra Samuels, A. Lacey Frommer, Wolf B. |
| description | Developing plant embryos depend on nutrition from maternal tissues via the seed coat and endosperm, but the mechanisms that supply nutrients to plant embryos have remained elusive. Sucrose, the major transport form of carbohydrate in plants, is delivered via the phloem to the maternal seed coat and then secreted from the seed coat to feed the embryo. Here, we show that seed filling in Arabidopsis thaliana requires the three sucrose transporters SWEET11, 12, and 15. SWEET11, 12, and 15 exhibit specific spatiotemporal expression patterns in developing seeds, but only a sweet11;12;15 triple mutant showed severe seed defects, which include retarded embryo development, reduced seed weight, and reduced starch and lipid content, causing a “wrinkled” seed phenotype. In sweet11;12;15 triple mutants, starch accumulated in the seed coat but not the embryo, implicating SWEET-mediated sucrose efflux in the transfer of sugars from seed coat to embryo. This cascade of sequentially expressed SWEETs provides the feeding pathway for the plant embryo, an important feature for yield potential. |
| doi_str_mv | 10.1105/tpc.114.134585 |
| format | Article |
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Lacey ; Frommer, Wolf B.</creator><creatorcontrib>Chen, Li-Qing ; Lin, I Winnie ; Qu, Xiao-Qing ; Sosso, Davide ; McFarlane, Heather E. ; Londoño, Alejandra ; Samuels, A. Lacey ; Frommer, Wolf B.</creatorcontrib><description>Developing plant embryos depend on nutrition from maternal tissues via the seed coat and endosperm, but the mechanisms that supply nutrients to plant embryos have remained elusive. Sucrose, the major transport form of carbohydrate in plants, is delivered via the phloem to the maternal seed coat and then secreted from the seed coat to feed the embryo. Here, we show that seed filling in Arabidopsis thaliana requires the three sucrose transporters SWEET11, 12, and 15. SWEET11, 12, and 15 exhibit specific spatiotemporal expression patterns in developing seeds, but only a sweet11;12;15 triple mutant showed severe seed defects, which include retarded embryo development, reduced seed weight, and reduced starch and lipid content, causing a “wrinkled” seed phenotype. In sweet11;12;15 triple mutants, starch accumulated in the seed coat but not the embryo, implicating SWEET-mediated sucrose efflux in the transfer of sugars from seed coat to embryo. This cascade of sequentially expressed SWEETs provides the feeding pathway for the plant embryo, an important feature for yield potential.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.114.134585</identifier><identifier>PMID: 25794936</identifier><language>eng</language><publisher>England: American Society of Plant Biologists</publisher><subject>Animals ; Arabidopsis ; Arabidopsis - drug effects ; Arabidopsis - embryology ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Biological Transport - drug effects ; Biological Transport - genetics ; Embryogenesis ; Embryos ; Endosperm ; Endosperm - genetics ; Endosperm - metabolism ; Gene Expression Regulation, Developmental - drug effects ; Gene Expression Regulation, Plant - drug effects ; Integument ; Membrane Transport Proteins - genetics ; Membrane Transport Proteins - metabolism ; Models, Biological ; mutants ; Mutation - genetics ; nutrition ; Nutritional Physiological Phenomena - drug effects ; Oocytes - metabolism ; Organ Specificity - drug effects ; Organ Specificity - genetics ; Phenotype ; Plant cells ; Plant Leaves - drug effects ; Plant Leaves - metabolism ; Plant Roots - drug effects ; Plant Roots - genetics ; Plant Roots - growth & development ; Plants ; seed coat ; seed yield ; Seeds ; Starch - metabolism ; Starches ; sucrose ; Sucrose - metabolism ; Sucrose - pharmacology ; Sugars ; Testa ; Time Factors ; tissues ; transporters ; Xenopus laevis</subject><ispartof>The Plant cell, 2015-03, Vol.27 (3), p.607-619</ispartof><rights>2015 American Society of Plant Biologists</rights><rights>2015 American Society of Plant Biologists. All rights reserved.</rights><rights>2015 American Society of Plant Biologists. All rights reserved. 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c554t-2782faa309b510652f6a997267939c0ce21874b2d1fc365b758e15c9f6cf2f073</citedby><orcidid>0000-0002-0964-5388</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/plantcell.27.3.607$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/plantcell.27.3.607$$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/25794936$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Li-Qing</creatorcontrib><creatorcontrib>Lin, I Winnie</creatorcontrib><creatorcontrib>Qu, Xiao-Qing</creatorcontrib><creatorcontrib>Sosso, Davide</creatorcontrib><creatorcontrib>McFarlane, Heather E.</creatorcontrib><creatorcontrib>Londoño, Alejandra</creatorcontrib><creatorcontrib>Samuels, A. Lacey</creatorcontrib><creatorcontrib>Frommer, Wolf B.</creatorcontrib><title>A Cascade of Sequentially Expressed Sucrose Transporters in the Seed Coat and Endosperm Provides Nutrition for the Arabidopsis Embryo</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>Developing plant embryos depend on nutrition from maternal tissues via the seed coat and endosperm, but the mechanisms that supply nutrients to plant embryos have remained elusive. Sucrose, the major transport form of carbohydrate in plants, is delivered via the phloem to the maternal seed coat and then secreted from the seed coat to feed the embryo. Here, we show that seed filling in Arabidopsis thaliana requires the three sucrose transporters SWEET11, 12, and 15. SWEET11, 12, and 15 exhibit specific spatiotemporal expression patterns in developing seeds, but only a sweet11;12;15 triple mutant showed severe seed defects, which include retarded embryo development, reduced seed weight, and reduced starch and lipid content, causing a “wrinkled” seed phenotype. In sweet11;12;15 triple mutants, starch accumulated in the seed coat but not the embryo, implicating SWEET-mediated sucrose efflux in the transfer of sugars from seed coat to embryo. This cascade of sequentially expressed SWEETs provides the feeding pathway for the plant embryo, an important feature for yield potential.</description><subject>Animals</subject><subject>Arabidopsis</subject><subject>Arabidopsis - drug effects</subject><subject>Arabidopsis - embryology</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Biological Transport - drug effects</subject><subject>Biological Transport - genetics</subject><subject>Embryogenesis</subject><subject>Embryos</subject><subject>Endosperm</subject><subject>Endosperm - genetics</subject><subject>Endosperm - metabolism</subject><subject>Gene Expression Regulation, Developmental - drug effects</subject><subject>Gene Expression Regulation, Plant - drug effects</subject><subject>Integument</subject><subject>Membrane Transport Proteins - genetics</subject><subject>Membrane Transport Proteins - metabolism</subject><subject>Models, Biological</subject><subject>mutants</subject><subject>Mutation - genetics</subject><subject>nutrition</subject><subject>Nutritional Physiological Phenomena - drug effects</subject><subject>Oocytes - metabolism</subject><subject>Organ Specificity - drug effects</subject><subject>Organ Specificity - genetics</subject><subject>Phenotype</subject><subject>Plant cells</subject><subject>Plant Leaves - drug effects</subject><subject>Plant Leaves - metabolism</subject><subject>Plant Roots - drug effects</subject><subject>Plant Roots - genetics</subject><subject>Plant Roots - growth & development</subject><subject>Plants</subject><subject>seed coat</subject><subject>seed yield</subject><subject>Seeds</subject><subject>Starch - metabolism</subject><subject>Starches</subject><subject>sucrose</subject><subject>Sucrose - metabolism</subject><subject>Sucrose - pharmacology</subject><subject>Sugars</subject><subject>Testa</subject><subject>Time Factors</subject><subject>tissues</subject><subject>transporters</subject><subject>Xenopus laevis</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUtv1DAUhS0EoqWwZYm8o5sMfsSvDdJoNDykCpBaJHaW49jUVRIH26mYH9D_XU-njGDFyke6372-9xwAXmO0whixd2W2VbQrTFsm2RNwihklDVHyx9OqUYualjN8Al7kfIMQwgKr5-CEMKFaRfkpuFvDjcnW9A5GDy_dr8VNJZhh2MHt7zm5nF0PLxebYnbwKpkpzzEVlzIMEyzXrrZUYBNNgWbq4XbqY55dGuG3FG9D7zL8spQUSogT9DE9tKyT6UIf5xwy3I5d2sWX4Jk3Q3avHt8z8P3D9mrzqbn4-vHzZn3RWMba0hAhiTeGItUxjDgjnhulBOFCUWWRdQRL0Xakx95SzjrBpMPMKs-tJx4JegbeH-bOSze63tZbkxn0nMJo0k5HE_S_lSlc65_xVreMSc5kHXD-OCDFalUuegzZumEwk4tL1uTBYyk5_S-KJZICU8R4RVcHdG9zTs4fN8JI72PWNeYqWn2IuTa8-fuOI_4n1wq8PQA3ucR0rM_187LfQROhqebVkntVILOp</recordid><startdate>20150301</startdate><enddate>20150301</enddate><creator>Chen, Li-Qing</creator><creator>Lin, I Winnie</creator><creator>Qu, Xiao-Qing</creator><creator>Sosso, Davide</creator><creator>McFarlane, Heather E.</creator><creator>Londoño, Alejandra</creator><creator>Samuels, A. Lacey</creator><creator>Frommer, Wolf B.</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>7QO</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0964-5388</orcidid></search><sort><creationdate>20150301</creationdate><title>A Cascade of Sequentially Expressed Sucrose Transporters in the Seed Coat and Endosperm Provides Nutrition for the Arabidopsis Embryo</title><author>Chen, Li-Qing ; Lin, I Winnie ; Qu, Xiao-Qing ; Sosso, Davide ; McFarlane, Heather E. ; Londoño, Alejandra ; Samuels, A. Lacey ; Frommer, Wolf B.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c554t-2782faa309b510652f6a997267939c0ce21874b2d1fc365b758e15c9f6cf2f073</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Arabidopsis</topic><topic>Arabidopsis - drug effects</topic><topic>Arabidopsis - embryology</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>Biological Transport - drug effects</topic><topic>Biological Transport - genetics</topic><topic>Embryogenesis</topic><topic>Embryos</topic><topic>Endosperm</topic><topic>Endosperm - genetics</topic><topic>Endosperm - metabolism</topic><topic>Gene Expression Regulation, Developmental - drug effects</topic><topic>Gene Expression Regulation, Plant - drug effects</topic><topic>Integument</topic><topic>Membrane Transport Proteins - genetics</topic><topic>Membrane Transport Proteins - metabolism</topic><topic>Models, Biological</topic><topic>mutants</topic><topic>Mutation - genetics</topic><topic>nutrition</topic><topic>Nutritional Physiological Phenomena - drug effects</topic><topic>Oocytes - metabolism</topic><topic>Organ Specificity - drug effects</topic><topic>Organ Specificity - genetics</topic><topic>Phenotype</topic><topic>Plant cells</topic><topic>Plant Leaves - drug effects</topic><topic>Plant Leaves - metabolism</topic><topic>Plant Roots - drug effects</topic><topic>Plant Roots - genetics</topic><topic>Plant Roots - growth & development</topic><topic>Plants</topic><topic>seed coat</topic><topic>seed yield</topic><topic>Seeds</topic><topic>Starch - metabolism</topic><topic>Starches</topic><topic>sucrose</topic><topic>Sucrose - metabolism</topic><topic>Sucrose - pharmacology</topic><topic>Sugars</topic><topic>Testa</topic><topic>Time Factors</topic><topic>tissues</topic><topic>transporters</topic><topic>Xenopus laevis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Li-Qing</creatorcontrib><creatorcontrib>Lin, I Winnie</creatorcontrib><creatorcontrib>Qu, Xiao-Qing</creatorcontrib><creatorcontrib>Sosso, Davide</creatorcontrib><creatorcontrib>McFarlane, Heather E.</creatorcontrib><creatorcontrib>Londoño, Alejandra</creatorcontrib><creatorcontrib>Samuels, A. Lacey</creatorcontrib><creatorcontrib>Frommer, Wolf B.</creatorcontrib><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>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>AGRICOLA</collection><collection>AGRICOLA - 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>Chen, Li-Qing</au><au>Lin, I Winnie</au><au>Qu, Xiao-Qing</au><au>Sosso, Davide</au><au>McFarlane, Heather E.</au><au>Londoño, Alejandra</au><au>Samuels, A. Lacey</au><au>Frommer, Wolf B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Cascade of Sequentially Expressed Sucrose Transporters in the Seed Coat and Endosperm Provides Nutrition for the Arabidopsis Embryo</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2015-03-01</date><risdate>2015</risdate><volume>27</volume><issue>3</issue><spage>607</spage><epage>619</epage><pages>607-619</pages><issn>1040-4651</issn><eissn>1532-298X</eissn><abstract>Developing plant embryos depend on nutrition from maternal tissues via the seed coat and endosperm, but the mechanisms that supply nutrients to plant embryos have remained elusive. Sucrose, the major transport form of carbohydrate in plants, is delivered via the phloem to the maternal seed coat and then secreted from the seed coat to feed the embryo. Here, we show that seed filling in Arabidopsis thaliana requires the three sucrose transporters SWEET11, 12, and 15. SWEET11, 12, and 15 exhibit specific spatiotemporal expression patterns in developing seeds, but only a sweet11;12;15 triple mutant showed severe seed defects, which include retarded embryo development, reduced seed weight, and reduced starch and lipid content, causing a “wrinkled” seed phenotype. In sweet11;12;15 triple mutants, starch accumulated in the seed coat but not the embryo, implicating SWEET-mediated sucrose efflux in the transfer of sugars from seed coat to embryo. This cascade of sequentially expressed SWEETs provides the feeding pathway for the plant embryo, an important feature for yield potential.</abstract><cop>England</cop><pub>American Society of Plant Biologists</pub><pmid>25794936</pmid><doi>10.1105/tpc.114.134585</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-0964-5388</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | The Plant cell, 2015-03, Vol.27 (3), p.607-619 |
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| language | eng |
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| source | Jstor Complete Legacy; Oxford University Press Journals All Titles (1996-Current); MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
| subjects | Animals Arabidopsis Arabidopsis - drug effects Arabidopsis - embryology Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana Biological Transport - drug effects Biological Transport - genetics Embryogenesis Embryos Endosperm Endosperm - genetics Endosperm - metabolism Gene Expression Regulation, Developmental - drug effects Gene Expression Regulation, Plant - drug effects Integument Membrane Transport Proteins - genetics Membrane Transport Proteins - metabolism Models, Biological mutants Mutation - genetics nutrition Nutritional Physiological Phenomena - drug effects Oocytes - metabolism Organ Specificity - drug effects Organ Specificity - genetics Phenotype Plant cells Plant Leaves - drug effects Plant Leaves - metabolism Plant Roots - drug effects Plant Roots - genetics Plant Roots - growth & development Plants seed coat seed yield Seeds Starch - metabolism Starches sucrose Sucrose - metabolism Sucrose - pharmacology Sugars Testa Time Factors tissues transporters Xenopus laevis |
| title | A Cascade of Sequentially Expressed Sucrose Transporters in the Seed Coat and Endosperm Provides Nutrition for the Arabidopsis Embryo |
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