Maize opaque10 Encodes a Cereal-Specific Protein That Is Essential for the Proper Distribution of Zeins in Endosperm Protein Bodies
Cereal storage proteins are major nitrogen sources for humans and livestock. Prolamins are the most abundant storage protein in most cereals. They are deposited into protein bodies (PBs) in seed endosperm. The inner structure and the storage mechanism for prolamin PBs is poorly understood. Maize opa...
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| description | Cereal storage proteins are major nitrogen sources for humans and livestock. Prolamins are the most abundant storage protein in most cereals. They are deposited into protein bodies (PBs) in seed endosperm. The inner structure and the storage mechanism for prolamin PBs is poorly understood. Maize opaque10 (o10) is a classic opaque endosperm mutant with misshapen PBs. Through positional cloning, we found that O10 encodes a novel cereal-specific PB protein. Its middle domain contains a seven-repeat sequence that is responsible for its dimerization. Its C terminus contains a transmembrane motif that is required for its ER localization and PB deposition. A cellular fractionation assay indicated that O10 is initially synthesized in the cytoplasm and then anchored to the ER and eventually deposited in the PB. O10 can interact with 19-kD and 22-kD α-zeins and 16-kD and 50-kD γ-zeins through its N-terminal domain. An immunolocalization assay indicated that O10 co-localizes with 16-kD γ-zein and 22-kD α-zein in PBs, forming a ring-shaped structure at the interface between the α-zein-rich core and the γ-zein-rich peripheral region. The loss of O10 function disrupts this ring-shaped distribution of 22-kD and 16-kD zeins, resulting in misshapen PBs. These results showed that O10, as a newly evolved PB protein, is essential for the ring-shaped distribution of 22-kD and 16-kD zeins and controls PB morphology in maize endosperm. |
| doi_str_mv | 10.1371/journal.pgen.1006270 |
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Prolamins are the most abundant storage protein in most cereals. They are deposited into protein bodies (PBs) in seed endosperm. The inner structure and the storage mechanism for prolamin PBs is poorly understood. Maize opaque10 (o10) is a classic opaque endosperm mutant with misshapen PBs. Through positional cloning, we found that O10 encodes a novel cereal-specific PB protein. Its middle domain contains a seven-repeat sequence that is responsible for its dimerization. Its C terminus contains a transmembrane motif that is required for its ER localization and PB deposition. A cellular fractionation assay indicated that O10 is initially synthesized in the cytoplasm and then anchored to the ER and eventually deposited in the PB. O10 can interact with 19-kD and 22-kD α-zeins and 16-kD and 50-kD γ-zeins through its N-terminal domain. An immunolocalization assay indicated that O10 co-localizes with 16-kD γ-zein and 22-kD α-zein in PBs, forming a ring-shaped structure at the interface between the α-zein-rich core and the γ-zein-rich peripheral region. The loss of O10 function disrupts this ring-shaped distribution of 22-kD and 16-kD zeins, resulting in misshapen PBs. These results showed that O10, as a newly evolved PB protein, is essential for the ring-shaped distribution of 22-kD and 16-kD zeins and controls PB morphology in maize endosperm.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1006270</identifier><identifier>PMID: 27541862</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Biology and Life Sciences ; Cloning ; Corn ; Edible Grain - genetics ; Edible Grain - growth & development ; Endosperm - genetics ; Endosperm - growth & development ; Funding ; Gene Expression Regulation, Plant ; Genetic aspects ; Localization ; Molecular weight ; Morphology ; Physical Sciences ; Physiological aspects ; Plant proteins ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants, Genetically Modified - genetics ; Plants, Genetically Modified - metabolism ; Proteins ; Research and Analysis Methods ; Seeds - genetics ; Seeds - growth & development ; Studies ; Zea mays ; Zea mays - genetics ; Zea mays - growth & development ; Zein - genetics ; Zein - metabolism</subject><ispartof>PLoS genetics, 2016-08, Vol.12 (8), p.e1006270-e1006270</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 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: Encodes a Cereal-Specific Protein That Is Essential for the Proper Distribution of Zeins in Endosperm Protein Bodies. PLoS Genet 12(8): e1006270. doi:10.1371/journal.pgen.1006270</rights><rights>2016 Yao et al 2016 Yao et al</rights><rights>2016 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: Encodes a Cereal-Specific Protein That Is Essential for the Proper Distribution of Zeins in Endosperm Protein Bodies. PLoS Genet 12(8): e1006270. doi:10.1371/journal.pgen.1006270</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c759t-7aa6b5aabb8a66009bb02e2dd28098fe2b81fd453c48526c4b141abd28b48603</citedby><cites>FETCH-LOGICAL-c759t-7aa6b5aabb8a66009bb02e2dd28098fe2b81fd453c48526c4b141abd28b48603</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4991801/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4991801/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27541862$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yao, Dongsheng</creatorcontrib><creatorcontrib>Qi, Weiwei</creatorcontrib><creatorcontrib>Li, Xia</creatorcontrib><creatorcontrib>Yang, Qing</creatorcontrib><creatorcontrib>Yan, Shumei</creatorcontrib><creatorcontrib>Ling, Huiling</creatorcontrib><creatorcontrib>Wang, Gang</creatorcontrib><creatorcontrib>Wang, Guifeng</creatorcontrib><creatorcontrib>Song, Rentao</creatorcontrib><title>Maize opaque10 Encodes a Cereal-Specific Protein That Is Essential for the Proper Distribution of Zeins in Endosperm Protein Bodies</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Cereal storage proteins are major nitrogen sources for humans and livestock. Prolamins are the most abundant storage protein in most cereals. They are deposited into protein bodies (PBs) in seed endosperm. The inner structure and the storage mechanism for prolamin PBs is poorly understood. Maize opaque10 (o10) is a classic opaque endosperm mutant with misshapen PBs. Through positional cloning, we found that O10 encodes a novel cereal-specific PB protein. Its middle domain contains a seven-repeat sequence that is responsible for its dimerization. Its C terminus contains a transmembrane motif that is required for its ER localization and PB deposition. A cellular fractionation assay indicated that O10 is initially synthesized in the cytoplasm and then anchored to the ER and eventually deposited in the PB. O10 can interact with 19-kD and 22-kD α-zeins and 16-kD and 50-kD γ-zeins through its N-terminal domain. An immunolocalization assay indicated that O10 co-localizes with 16-kD γ-zein and 22-kD α-zein in PBs, forming a ring-shaped structure at the interface between the α-zein-rich core and the γ-zein-rich peripheral region. The loss of O10 function disrupts this ring-shaped distribution of 22-kD and 16-kD zeins, resulting in misshapen PBs. These results showed that O10, as a newly evolved PB protein, is essential for the ring-shaped distribution of 22-kD and 16-kD zeins and controls PB morphology in maize endosperm.</description><subject>Biology and Life Sciences</subject><subject>Cloning</subject><subject>Corn</subject><subject>Edible Grain - genetics</subject><subject>Edible Grain - growth & development</subject><subject>Endosperm - genetics</subject><subject>Endosperm - growth & development</subject><subject>Funding</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genetic aspects</subject><subject>Localization</subject><subject>Molecular weight</subject><subject>Morphology</subject><subject>Physical Sciences</subject><subject>Physiological aspects</subject><subject>Plant proteins</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Plants, Genetically Modified - metabolism</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Seeds - genetics</subject><subject>Seeds - growth & development</subject><subject>Studies</subject><subject>Zea mays</subject><subject>Zea mays - genetics</subject><subject>Zea mays - growth & development</subject><subject>Zein - genetics</subject><subject>Zein - metabolism</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVk0GPEyEUxydG466r38AoiYnRQyswMAMXk7VWbbK6xm08eCEM86almQ4VZox69YtL29mmY_awhgMEfv__g_d4SfKY4DFJc_Jq5Trf6Hq8WUAzJhhnNMd3klPCeTrKGWZ3j9YnyYMQVhinXMj8fnJCc86IyOhp8uejtr8BuY3-3gHBaNoYV0JAGk3Ag65HVxswtrIGffauBdug-VK3aBbQNARoWqtrVDmP2iVsiQ149NaG1tuia61rkKvQt6gKKCqnTelCJNYHrzeutBAeJvcqXQd41M9nyfzddD75MLq4fD-bnF-MTM5lO8q1zgqudVEInWUYy6LAFGhZUoGlqIAWglQl46lhgtPMsIIwoot4XDCR4fQsebq33dQuqD59QRFBMRWcZTISsz1ROr1SG2_X2v9STlu123B-obRvralBCSJFmrGUE2xiSCKYpMCgpJRkAIJEr9d9tK5YQ2lirryuB6bDk8Yu1cL9UExKIvDW4EVv4F2sTWjV2gYDda0bcN3u3rmQXObpLVCSZlRinkf02T_ozYnoqYWOb7VN5eIVzdZUnbNcMszTlEZqfAMVRwlra1wDlY37A8HLgSAyLfxsF7oLQc2uvvwH--n27OXXIfv8iF3GL94ug6t3vzUMQbYHjXcheKgOtSNYbTvwOnNq24Gq78Aoe3Jc94PouuXSv6-WKLc</recordid><startdate>20160819</startdate><enddate>20160819</enddate><creator>Yao, Dongsheng</creator><creator>Qi, Weiwei</creator><creator>Li, Xia</creator><creator>Yang, Qing</creator><creator>Yan, Shumei</creator><creator>Ling, Huiling</creator><creator>Wang, Gang</creator><creator>Wang, Guifeng</creator><creator>Song, Rentao</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>IOV</scope><scope>ISN</scope><scope>ISR</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>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160819</creationdate><title>Maize opaque10 Encodes a Cereal-Specific Protein That Is Essential for the Proper Distribution of Zeins in Endosperm Protein Bodies</title><author>Yao, Dongsheng ; Qi, Weiwei ; Li, Xia ; Yang, Qing ; Yan, Shumei ; Ling, Huiling ; Wang, Gang ; Wang, Guifeng ; Song, Rentao</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c759t-7aa6b5aabb8a66009bb02e2dd28098fe2b81fd453c48526c4b141abd28b48603</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Biology and Life Sciences</topic><topic>Cloning</topic><topic>Corn</topic><topic>Edible Grain - genetics</topic><topic>Edible Grain - growth & development</topic><topic>Endosperm - genetics</topic><topic>Endosperm - growth & development</topic><topic>Funding</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genetic aspects</topic><topic>Localization</topic><topic>Molecular weight</topic><topic>Morphology</topic><topic>Physical Sciences</topic><topic>Physiological aspects</topic><topic>Plant proteins</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants, Genetically Modified - genetics</topic><topic>Plants, Genetically Modified - metabolism</topic><topic>Proteins</topic><topic>Research and Analysis Methods</topic><topic>Seeds - genetics</topic><topic>Seeds - growth & development</topic><topic>Studies</topic><topic>Zea mays</topic><topic>Zea mays - genetics</topic><topic>Zea mays - growth & development</topic><topic>Zein - genetics</topic><topic>Zein - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yao, Dongsheng</creatorcontrib><creatorcontrib>Qi, Weiwei</creatorcontrib><creatorcontrib>Li, Xia</creatorcontrib><creatorcontrib>Yang, Qing</creatorcontrib><creatorcontrib>Yan, Shumei</creatorcontrib><creatorcontrib>Ling, Huiling</creatorcontrib><creatorcontrib>Wang, Gang</creatorcontrib><creatorcontrib>Wang, Guifeng</creatorcontrib><creatorcontrib>Song, Rentao</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</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>MEDLINE - Academic</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>Yao, Dongsheng</au><au>Qi, Weiwei</au><au>Li, Xia</au><au>Yang, Qing</au><au>Yan, Shumei</au><au>Ling, Huiling</au><au>Wang, Gang</au><au>Wang, Guifeng</au><au>Song, Rentao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Maize opaque10 Encodes a Cereal-Specific Protein That Is Essential for the Proper Distribution of Zeins in Endosperm Protein Bodies</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2016-08-19</date><risdate>2016</risdate><volume>12</volume><issue>8</issue><spage>e1006270</spage><epage>e1006270</epage><pages>e1006270-e1006270</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Cereal storage proteins are major nitrogen sources for humans and livestock. Prolamins are the most abundant storage protein in most cereals. They are deposited into protein bodies (PBs) in seed endosperm. The inner structure and the storage mechanism for prolamin PBs is poorly understood. Maize opaque10 (o10) is a classic opaque endosperm mutant with misshapen PBs. Through positional cloning, we found that O10 encodes a novel cereal-specific PB protein. Its middle domain contains a seven-repeat sequence that is responsible for its dimerization. Its C terminus contains a transmembrane motif that is required for its ER localization and PB deposition. A cellular fractionation assay indicated that O10 is initially synthesized in the cytoplasm and then anchored to the ER and eventually deposited in the PB. O10 can interact with 19-kD and 22-kD α-zeins and 16-kD and 50-kD γ-zeins through its N-terminal domain. An immunolocalization assay indicated that O10 co-localizes with 16-kD γ-zein and 22-kD α-zein in PBs, forming a ring-shaped structure at the interface between the α-zein-rich core and the γ-zein-rich peripheral region. The loss of O10 function disrupts this ring-shaped distribution of 22-kD and 16-kD zeins, resulting in misshapen PBs. These results showed that O10, as a newly evolved PB protein, is essential for the ring-shaped distribution of 22-kD and 16-kD zeins and controls PB morphology in maize endosperm.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27541862</pmid><doi>10.1371/journal.pgen.1006270</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Biology and Life Sciences Cloning Corn Edible Grain - genetics Edible Grain - growth & development Endosperm - genetics Endosperm - growth & development Funding Gene Expression Regulation, Plant Genetic aspects Localization Molecular weight Morphology Physical Sciences Physiological aspects Plant proteins Plant Proteins - genetics Plant Proteins - metabolism Plants, Genetically Modified - genetics Plants, Genetically Modified - metabolism Proteins Research and Analysis Methods Seeds - genetics Seeds - growth & development Studies Zea mays Zea mays - genetics Zea mays - growth & development Zein - genetics Zein - metabolism |
| title | Maize opaque10 Encodes a Cereal-Specific Protein That Is Essential for the Proper Distribution of Zeins in Endosperm Protein Bodies |
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