DCT4—A New Member of the Dicarboxylate Transporter Family in C4 Grasses
Abstract Malate transport shuttles atmospheric carbon into the Calvin–Benson cycle during NADP-ME C4 photosynthesis. Previous characterizations of several plant dicarboxylate transporters (DCT) showed that they efficiently exchange malate across membranes. Here, we identify and characterize a previo...
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| Veröffentlicht in: | Genome biology and evolution 2021-02, Vol.13 (2) |
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| creator | Weissmann, Sarit Huang, Pu Wiechert, Madeline A Furuyama, Koki Brutnell, Thomas P Taniguchi, Mitsutaka Schnable, James C Mockler, Todd C |
| description | Abstract
Malate transport shuttles atmospheric carbon into the Calvin–Benson cycle during NADP-ME C4 photosynthesis. Previous characterizations of several plant dicarboxylate transporters (DCT) showed that they efficiently exchange malate across membranes. Here, we identify and characterize a previously unknown member of the DCT family, DCT4, in Sorghum bicolor. We show that SbDCT4 exchanges malate across membranes and its expression pattern is consistent with a role in malate transport during C4 photosynthesis. SbDCT4 is not syntenic to the characterized photosynthetic gene ZmDCT2, and an ortholog is not detectable in the maize reference genome. We found that the expression patterns of DCT family genes in the leaves of Zea mays, and S. bicolor varied by cell type. Our results suggest that subfunctionalization, of members of the DCT family, for the transport of malate into the bundle sheath plastids, occurred during the process of independent recurrent evolution of C4 photosynthesis in grasses of the PACMAD clade. We also show that this subfunctionalization is lineage independent. Our results challenge the dogma that key C4 genes must be orthologues of one another among C4 species, and shed new light on the evolution of C4 photosynthesis. |
| doi_str_mv | 10.1093/gbe/evaa251 |
| format | Article |
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Malate transport shuttles atmospheric carbon into the Calvin–Benson cycle during NADP-ME C4 photosynthesis. Previous characterizations of several plant dicarboxylate transporters (DCT) showed that they efficiently exchange malate across membranes. Here, we identify and characterize a previously unknown member of the DCT family, DCT4, in Sorghum bicolor. We show that SbDCT4 exchanges malate across membranes and its expression pattern is consistent with a role in malate transport during C4 photosynthesis. SbDCT4 is not syntenic to the characterized photosynthetic gene ZmDCT2, and an ortholog is not detectable in the maize reference genome. We found that the expression patterns of DCT family genes in the leaves of Zea mays, and S. bicolor varied by cell type. Our results suggest that subfunctionalization, of members of the DCT family, for the transport of malate into the bundle sheath plastids, occurred during the process of independent recurrent evolution of C4 photosynthesis in grasses of the PACMAD clade. We also show that this subfunctionalization is lineage independent. Our results challenge the dogma that key C4 genes must be orthologues of one another among C4 species, and shed new light on the evolution of C4 photosynthesis.</description><identifier>ISSN: 1759-6653</identifier><identifier>EISSN: 1759-6653</identifier><identifier>DOI: 10.1093/gbe/evaa251</identifier><identifier>PMID: 33587128</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>BASIC BIOLOGICAL SCIENCES ; C4 photosynthesis ; DCT4 ; Dicarboxylic Acid Transporters - classification ; Dicarboxylic Acid Transporters - genetics ; Dicarboxylic Acid Transporters - metabolism ; Genes, Plant ; grass evolution ; Letter ; Malates - metabolism ; Multigene Family ; new transporter gene ; Phylogeny ; Plant Proteins - classification ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Sorghum - genetics ; Sorghum - metabolism</subject><ispartof>Genome biology and evolution, 2021-02, Vol.13 (2)</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 2021</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.</rights><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3541-c2f6c62a078ab04d6c5fe715f55ed3f0b12ef344a39d49c5b4721fb7eb9918e73</citedby><cites>FETCH-LOGICAL-c3541-c2f6c62a078ab04d6c5fe715f55ed3f0b12ef344a39d49c5b4721fb7eb9918e73</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/PMC7883667/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7883667/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,1605,27929,27930,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33587128$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1797387$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><contributor>Eyre-Walker, Adam</contributor><creatorcontrib>Weissmann, Sarit</creatorcontrib><creatorcontrib>Huang, Pu</creatorcontrib><creatorcontrib>Wiechert, Madeline A</creatorcontrib><creatorcontrib>Furuyama, Koki</creatorcontrib><creatorcontrib>Brutnell, Thomas P</creatorcontrib><creatorcontrib>Taniguchi, Mitsutaka</creatorcontrib><creatorcontrib>Schnable, James C</creatorcontrib><creatorcontrib>Mockler, Todd C</creatorcontrib><creatorcontrib>Donald Danforth Plant Science Center, St. Louis, MO (United States)</creatorcontrib><title>DCT4—A New Member of the Dicarboxylate Transporter Family in C4 Grasses</title><title>Genome biology and evolution</title><addtitle>Genome Biol Evol</addtitle><description>Abstract
Malate transport shuttles atmospheric carbon into the Calvin–Benson cycle during NADP-ME C4 photosynthesis. Previous characterizations of several plant dicarboxylate transporters (DCT) showed that they efficiently exchange malate across membranes. Here, we identify and characterize a previously unknown member of the DCT family, DCT4, in Sorghum bicolor. We show that SbDCT4 exchanges malate across membranes and its expression pattern is consistent with a role in malate transport during C4 photosynthesis. SbDCT4 is not syntenic to the characterized photosynthetic gene ZmDCT2, and an ortholog is not detectable in the maize reference genome. We found that the expression patterns of DCT family genes in the leaves of Zea mays, and S. bicolor varied by cell type. Our results suggest that subfunctionalization, of members of the DCT family, for the transport of malate into the bundle sheath plastids, occurred during the process of independent recurrent evolution of C4 photosynthesis in grasses of the PACMAD clade. We also show that this subfunctionalization is lineage independent. Our results challenge the dogma that key C4 genes must be orthologues of one another among C4 species, and shed new light on the evolution of C4 photosynthesis.</description><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>C4 photosynthesis</subject><subject>DCT4</subject><subject>Dicarboxylic Acid Transporters - classification</subject><subject>Dicarboxylic Acid Transporters - genetics</subject><subject>Dicarboxylic Acid Transporters - metabolism</subject><subject>Genes, Plant</subject><subject>grass evolution</subject><subject>Letter</subject><subject>Malates - metabolism</subject><subject>Multigene Family</subject><subject>new transporter gene</subject><subject>Phylogeny</subject><subject>Plant Proteins - classification</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Sorghum - genetics</subject><subject>Sorghum - metabolism</subject><issn>1759-6653</issn><issn>1759-6653</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNp9kctqGzEUhkVJaG5ddV9EFyUQ3Eij22hTCM4V0mTjrIUkH8UqMyNXGifxrg_RJ8yTZIzdkG6yOgfOx39--BD6TMl3SjQ7vndwDA_WVoJ-QLtUCT2SUrCtN_sO2ivlFyFScsk-oh3GRK1oVe-iq9PxhD__-XuCb-AR_4TWQcYp4H4G-DR6m116Wja2BzzJtivzlPsBOLdtbJY4dnjM8UW2pUA5QNvBNgU-beY-ujs_m4wvR9e3F1fjk-uRZ4LTka-C9LKyRNXWET6VXgRQVAQhYMoCcbSCwDi3TE-59sJxVdHgFDitaQ2K7aMf69z5wrUw9dD12TZmnmNr89IkG83_ly7OzH16MKqumZSrgK_rgFT6aIqPPfiZT10HvjdUacXqFXS4-ZLT7wWU3rSxeGga20FaFFPxWgutGSUDerRGfU6lZAivXSgxK0NmMGQ2hgb6y9v6r-w_JQPwbVNvMX836QWHmpp8</recordid><startdate>20210203</startdate><enddate>20210203</enddate><creator>Weissmann, Sarit</creator><creator>Huang, Pu</creator><creator>Wiechert, Madeline A</creator><creator>Furuyama, Koki</creator><creator>Brutnell, Thomas P</creator><creator>Taniguchi, Mitsutaka</creator><creator>Schnable, James C</creator><creator>Mockler, Todd C</creator><general>Oxford University Press</general><general>Society for Molecular Biology and Evolution</general><scope>TOX</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>7X8</scope><scope>OIOZB</scope><scope>OTOTI</scope><scope>5PM</scope></search><sort><creationdate>20210203</creationdate><title>DCT4—A New Member of the Dicarboxylate Transporter Family in C4 Grasses</title><author>Weissmann, Sarit ; Huang, Pu ; Wiechert, Madeline A ; Furuyama, Koki ; Brutnell, Thomas P ; Taniguchi, Mitsutaka ; Schnable, James C ; Mockler, Todd C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3541-c2f6c62a078ab04d6c5fe715f55ed3f0b12ef344a39d49c5b4721fb7eb9918e73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>C4 photosynthesis</topic><topic>DCT4</topic><topic>Dicarboxylic Acid Transporters - classification</topic><topic>Dicarboxylic Acid Transporters - genetics</topic><topic>Dicarboxylic Acid Transporters - metabolism</topic><topic>Genes, Plant</topic><topic>grass evolution</topic><topic>Letter</topic><topic>Malates - metabolism</topic><topic>Multigene Family</topic><topic>new transporter gene</topic><topic>Phylogeny</topic><topic>Plant Proteins - classification</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Sorghum - genetics</topic><topic>Sorghum - metabolism</topic><toplevel>online_resources</toplevel><creatorcontrib>Weissmann, Sarit</creatorcontrib><creatorcontrib>Huang, Pu</creatorcontrib><creatorcontrib>Wiechert, Madeline A</creatorcontrib><creatorcontrib>Furuyama, Koki</creatorcontrib><creatorcontrib>Brutnell, Thomas P</creatorcontrib><creatorcontrib>Taniguchi, Mitsutaka</creatorcontrib><creatorcontrib>Schnable, James C</creatorcontrib><creatorcontrib>Mockler, Todd C</creatorcontrib><creatorcontrib>Donald Danforth Plant Science Center, St. Louis, MO (United States)</creatorcontrib><collection>Access via Oxford University Press (Open Access Collection)</collection><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>OSTI.GOV - Hybrid</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genome biology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Weissmann, Sarit</au><au>Huang, Pu</au><au>Wiechert, Madeline A</au><au>Furuyama, Koki</au><au>Brutnell, Thomas P</au><au>Taniguchi, Mitsutaka</au><au>Schnable, James C</au><au>Mockler, Todd C</au><au>Eyre-Walker, Adam</au><aucorp>Donald Danforth Plant Science Center, St. Louis, MO (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>DCT4—A New Member of the Dicarboxylate Transporter Family in C4 Grasses</atitle><jtitle>Genome biology and evolution</jtitle><addtitle>Genome Biol Evol</addtitle><date>2021-02-03</date><risdate>2021</risdate><volume>13</volume><issue>2</issue><issn>1759-6653</issn><eissn>1759-6653</eissn><abstract>Abstract
Malate transport shuttles atmospheric carbon into the Calvin–Benson cycle during NADP-ME C4 photosynthesis. Previous characterizations of several plant dicarboxylate transporters (DCT) showed that they efficiently exchange malate across membranes. Here, we identify and characterize a previously unknown member of the DCT family, DCT4, in Sorghum bicolor. We show that SbDCT4 exchanges malate across membranes and its expression pattern is consistent with a role in malate transport during C4 photosynthesis. SbDCT4 is not syntenic to the characterized photosynthetic gene ZmDCT2, and an ortholog is not detectable in the maize reference genome. We found that the expression patterns of DCT family genes in the leaves of Zea mays, and S. bicolor varied by cell type. Our results suggest that subfunctionalization, of members of the DCT family, for the transport of malate into the bundle sheath plastids, occurred during the process of independent recurrent evolution of C4 photosynthesis in grasses of the PACMAD clade. We also show that this subfunctionalization is lineage independent. Our results challenge the dogma that key C4 genes must be orthologues of one another among C4 species, and shed new light on the evolution of C4 photosynthesis.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>33587128</pmid><doi>10.1093/gbe/evaa251</doi><oa>free_for_read</oa></addata></record> |
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| subjects | BASIC BIOLOGICAL SCIENCES C4 photosynthesis DCT4 Dicarboxylic Acid Transporters - classification Dicarboxylic Acid Transporters - genetics Dicarboxylic Acid Transporters - metabolism Genes, Plant grass evolution Letter Malates - metabolism Multigene Family new transporter gene Phylogeny Plant Proteins - classification Plant Proteins - genetics Plant Proteins - metabolism Sorghum - genetics Sorghum - metabolism |
| title | DCT4—A New Member of the Dicarboxylate Transporter Family in C4 Grasses |
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