Six-rowed spike4 (Vrs4) controls spikelet determinacy and row-type in barley
Inflorescence architecture of barley (Hordeum vulgare L.) is common among the Triticeae species, which bear one to three singleflowered spikelets at each rachis internode. Triple spikelet meristem is one of the unique features of barley spikes, in which three spikelets (one central and two lateral s...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2013-08, Vol.110 (32), p.13198-13203 |
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creator | Koppolu, Ravi Anwar, Nadia Sakuma, Shun Tagiri, Akemi Lundqvist, Udda Pourkheirandish, Mohammad Rutten, Twan Seiler, Christiane Himmelbach, Axel Ariyadasa, Ruvini Youssef, Helmy Mohamad Stein, Nils Sreenivasulu, Nese Komatsuda, Takao Schnurbusch, Thorsten |
description | Inflorescence architecture of barley (Hordeum vulgare L.) is common among the Triticeae species, which bear one to three singleflowered spikelets at each rachis internode. Triple spikelet meristem is one of the unique features of barley spikes, in which three spikelets (one central and two lateral spikelets) are produced at each rachis internode. Fertility of the lateral spikelets at triple spikelet meristem gives row-type identity to barley spikes. Sixrowed spikes show fertile lateral spikelets and produce increased grain yield per spike, compared with two-rowed spikes with sterile lateral spikelets. Thus, far, two loci governing the row-type phenotype were isolated in barley that include Six-rowed spikei (Vrs1) and Intermedium-C. In the present study, we isolated Six-rowed spike4 (Vrs4), a barley ortholog of the maize (Zea mays L.) inflorescence architecture gene RAMOSA2 (RA2). Eighteen coding mutations in barley RA2 (HvRA2) were specifically associated with lateral spikelet fertility and loss of spikelet determinacy. Expression analyses through mRNA in situ hybridization and microarray showed that Vrs4 (HvRA2) controls the row-type pathway through Vrs1 (HvHox1) a negative regulator of lateral spikelet fertility in barley. Moreover, Vrs4 may also regulate transcripts of barley SISTER OF RAMOSA3 (HvSRA), a putative trehalose-6-phosphate phosphatase involved in trehalose-6-phosphate homeostasis implicated to control spikelet determinacy. Our expression data illustrated that, although RA2 is conserved among different grass species, its down-stream target genes appear to be modified in barley and possibly other species of tribe Triticeae. |
doi_str_mv | 10.1073/pnas.1221950110 |
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Triple spikelet meristem is one of the unique features of barley spikes, in which three spikelets (one central and two lateral spikelets) are produced at each rachis internode. Fertility of the lateral spikelets at triple spikelet meristem gives row-type identity to barley spikes. Sixrowed spikes show fertile lateral spikelets and produce increased grain yield per spike, compared with two-rowed spikes with sterile lateral spikelets. Thus, far, two loci governing the row-type phenotype were isolated in barley that include Six-rowed spikei (Vrs1) and Intermedium-C. In the present study, we isolated Six-rowed spike4 (Vrs4), a barley ortholog of the maize (Zea mays L.) inflorescence architecture gene RAMOSA2 (RA2). Eighteen coding mutations in barley RA2 (HvRA2) were specifically associated with lateral spikelet fertility and loss of spikelet determinacy. Expression analyses through mRNA in situ hybridization and microarray showed that Vrs4 (HvRA2) controls the row-type pathway through Vrs1 (HvHox1) a negative regulator of lateral spikelet fertility in barley. Moreover, Vrs4 may also regulate transcripts of barley SISTER OF RAMOSA3 (HvSRA), a putative trehalose-6-phosphate phosphatase involved in trehalose-6-phosphate homeostasis implicated to control spikelet determinacy. Our expression data illustrated that, although RA2 is conserved among different grass species, its down-stream target genes appear to be modified in barley and possibly other species of tribe Triticeae.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1221950110</identifier><identifier>PMID: 23878219</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Alleles ; Amino Acid Sequence ; Barley ; Base Sequence ; Biological Sciences ; Chromosome Mapping ; Chromosomes, Plant - genetics ; Corn ; Cytokinins ; Determinacy ; Fertility - genetics ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation, Plant ; Genes ; Genotype & phenotype ; grain yield ; grasses ; Haplotypes ; Homeostasis ; Hordeum - genetics ; Hordeum - metabolism ; Hordeum - ultrastructure ; Hordeum vulgare ; in situ hybridization ; Inflorescence - genetics ; Inflorescence - metabolism ; Inflorescence - ultrastructure ; Inflorescences ; loci ; Meristems ; messenger RNA ; microarray technology ; Microscopy, Electron, Scanning ; Molecular Sequence Data ; Mutation ; Nonnative species ; Oligonucleotide Array Sequence Analysis ; Phenotype ; Phenotypes ; Phylogeny ; Plant Proteins - classification ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Reverse Transcriptase Polymerase Chain Reaction ; Sequence Homology, Amino Acid ; Spikelets ; Zea mays</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2013-08, Vol.110 (32), p.13198-13203</ispartof><rights>copyright © 1993-2008 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Aug 6, 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c567t-aca9cae4656e38463dc5fcc4c6c22fcccbbbb409daddfdcf8308a50a7748042e3</citedby><cites>FETCH-LOGICAL-c567t-aca9cae4656e38463dc5fcc4c6c22fcccbbbb409daddfdcf8308a50a7748042e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/110/32.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/42712866$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/42712866$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23878219$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Koppolu, Ravi</creatorcontrib><creatorcontrib>Anwar, Nadia</creatorcontrib><creatorcontrib>Sakuma, Shun</creatorcontrib><creatorcontrib>Tagiri, Akemi</creatorcontrib><creatorcontrib>Lundqvist, Udda</creatorcontrib><creatorcontrib>Pourkheirandish, Mohammad</creatorcontrib><creatorcontrib>Rutten, Twan</creatorcontrib><creatorcontrib>Seiler, Christiane</creatorcontrib><creatorcontrib>Himmelbach, Axel</creatorcontrib><creatorcontrib>Ariyadasa, Ruvini</creatorcontrib><creatorcontrib>Youssef, Helmy Mohamad</creatorcontrib><creatorcontrib>Stein, Nils</creatorcontrib><creatorcontrib>Sreenivasulu, Nese</creatorcontrib><creatorcontrib>Komatsuda, Takao</creatorcontrib><creatorcontrib>Schnurbusch, Thorsten</creatorcontrib><title>Six-rowed spike4 (Vrs4) controls spikelet determinacy and row-type in barley</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Inflorescence architecture of barley (Hordeum vulgare L.) is common among the Triticeae species, which bear one to three singleflowered spikelets at each rachis internode. Triple spikelet meristem is one of the unique features of barley spikes, in which three spikelets (one central and two lateral spikelets) are produced at each rachis internode. Fertility of the lateral spikelets at triple spikelet meristem gives row-type identity to barley spikes. Sixrowed spikes show fertile lateral spikelets and produce increased grain yield per spike, compared with two-rowed spikes with sterile lateral spikelets. Thus, far, two loci governing the row-type phenotype were isolated in barley that include Six-rowed spikei (Vrs1) and Intermedium-C. In the present study, we isolated Six-rowed spike4 (Vrs4), a barley ortholog of the maize (Zea mays L.) inflorescence architecture gene RAMOSA2 (RA2). Eighteen coding mutations in barley RA2 (HvRA2) were specifically associated with lateral spikelet fertility and loss of spikelet determinacy. Expression analyses through mRNA in situ hybridization and microarray showed that Vrs4 (HvRA2) controls the row-type pathway through Vrs1 (HvHox1) a negative regulator of lateral spikelet fertility in barley. Moreover, Vrs4 may also regulate transcripts of barley SISTER OF RAMOSA3 (HvSRA), a putative trehalose-6-phosphate phosphatase involved in trehalose-6-phosphate homeostasis implicated to control spikelet determinacy. Our expression data illustrated that, although RA2 is conserved among different grass species, its down-stream target genes appear to be modified in barley and possibly other species of tribe Triticeae.</description><subject>Alleles</subject><subject>Amino Acid Sequence</subject><subject>Barley</subject><subject>Base Sequence</subject><subject>Biological Sciences</subject><subject>Chromosome Mapping</subject><subject>Chromosomes, Plant - genetics</subject><subject>Corn</subject><subject>Cytokinins</subject><subject>Determinacy</subject><subject>Fertility - genetics</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Genotype & phenotype</subject><subject>grain yield</subject><subject>grasses</subject><subject>Haplotypes</subject><subject>Homeostasis</subject><subject>Hordeum - genetics</subject><subject>Hordeum - metabolism</subject><subject>Hordeum - ultrastructure</subject><subject>Hordeum vulgare</subject><subject>in situ hybridization</subject><subject>Inflorescence - genetics</subject><subject>Inflorescence - metabolism</subject><subject>Inflorescence - ultrastructure</subject><subject>Inflorescences</subject><subject>loci</subject><subject>Meristems</subject><subject>messenger RNA</subject><subject>microarray technology</subject><subject>Microscopy, Electron, Scanning</subject><subject>Molecular Sequence Data</subject><subject>Mutation</subject><subject>Nonnative species</subject><subject>Oligonucleotide Array Sequence Analysis</subject><subject>Phenotype</subject><subject>Phenotypes</subject><subject>Phylogeny</subject><subject>Plant Proteins - classification</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Sequence Homology, Amino Acid</subject><subject>Spikelets</subject><subject>Zea mays</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUtvEzEUhS0Eomlh3RXIEpuymPb6MX5skFDVlkqRuiiwtRzbUyZMxoM9oc2_x6OElLKpN7bs7xzd44PQMYFTApKdDb3Np4RSomsgBF6gGQFNKsE1vEQzACorxSk_QIc5LwFA1wpeowPKlFRFNEPz2_ahSvE-eJyH9mfg-OR7yvwjdrEfU-zy9roLI_ZhDGnV9tZtsO09Lqpq3AwBtz1e2NSFzRv0qrFdDm93-xH6dnnx9fxLNb-5uj7_PK9cLeRYWWe1s4GLWgSmuGDe1Y1z3AlHaTm4RVkctLfeN941ioGyNVgpuQJOAztCn7a-w3qxCt6FMqrtzJDalU0bE21rnr707Q9zF38bJjkoLovByc4gxV_rkEezarMLXWf7ENfZEAUMNFVCPY9yogQXpYyCfvgPXcZ16stPTJSWSlExUWdbyqWYcwrNfm4CZirVTKWax1KL4v2_cff83xYLgHfApNzbFT9GDWFETzHebZFlHmPaM5xKUmIK9geSA7Jk</recordid><startdate>20130806</startdate><enddate>20130806</enddate><creator>Koppolu, Ravi</creator><creator>Anwar, Nadia</creator><creator>Sakuma, Shun</creator><creator>Tagiri, Akemi</creator><creator>Lundqvist, Udda</creator><creator>Pourkheirandish, Mohammad</creator><creator>Rutten, Twan</creator><creator>Seiler, Christiane</creator><creator>Himmelbach, Axel</creator><creator>Ariyadasa, Ruvini</creator><creator>Youssef, Helmy Mohamad</creator><creator>Stein, Nils</creator><creator>Sreenivasulu, Nese</creator><creator>Komatsuda, Takao</creator><creator>Schnurbusch, Thorsten</creator><general>National Academy of Sciences</general><general>National Acad Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</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>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20130806</creationdate><title>Six-rowed spike4 (Vrs4) controls spikelet determinacy and row-type in barley</title><author>Koppolu, Ravi ; Anwar, Nadia ; Sakuma, Shun ; Tagiri, Akemi ; Lundqvist, Udda ; Pourkheirandish, Mohammad ; Rutten, Twan ; Seiler, Christiane ; Himmelbach, Axel ; Ariyadasa, Ruvini ; Youssef, Helmy Mohamad ; Stein, Nils ; Sreenivasulu, Nese ; Komatsuda, Takao ; Schnurbusch, Thorsten</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c567t-aca9cae4656e38463dc5fcc4c6c22fcccbbbb409daddfdcf8308a50a7748042e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Alleles</topic><topic>Amino Acid Sequence</topic><topic>Barley</topic><topic>Base Sequence</topic><topic>Biological Sciences</topic><topic>Chromosome Mapping</topic><topic>Chromosomes, Plant - genetics</topic><topic>Corn</topic><topic>Cytokinins</topic><topic>Determinacy</topic><topic>Fertility - genetics</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genes</topic><topic>Genotype & phenotype</topic><topic>grain yield</topic><topic>grasses</topic><topic>Haplotypes</topic><topic>Homeostasis</topic><topic>Hordeum - genetics</topic><topic>Hordeum - metabolism</topic><topic>Hordeum - ultrastructure</topic><topic>Hordeum vulgare</topic><topic>in situ hybridization</topic><topic>Inflorescence - genetics</topic><topic>Inflorescence - metabolism</topic><topic>Inflorescence - ultrastructure</topic><topic>Inflorescences</topic><topic>loci</topic><topic>Meristems</topic><topic>messenger RNA</topic><topic>microarray technology</topic><topic>Microscopy, Electron, Scanning</topic><topic>Molecular Sequence Data</topic><topic>Mutation</topic><topic>Nonnative species</topic><topic>Oligonucleotide Array Sequence Analysis</topic><topic>Phenotype</topic><topic>Phenotypes</topic><topic>Phylogeny</topic><topic>Plant Proteins - classification</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>Sequence Homology, Amino Acid</topic><topic>Spikelets</topic><topic>Zea mays</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Koppolu, Ravi</creatorcontrib><creatorcontrib>Anwar, Nadia</creatorcontrib><creatorcontrib>Sakuma, Shun</creatorcontrib><creatorcontrib>Tagiri, Akemi</creatorcontrib><creatorcontrib>Lundqvist, Udda</creatorcontrib><creatorcontrib>Pourkheirandish, Mohammad</creatorcontrib><creatorcontrib>Rutten, Twan</creatorcontrib><creatorcontrib>Seiler, Christiane</creatorcontrib><creatorcontrib>Himmelbach, Axel</creatorcontrib><creatorcontrib>Ariyadasa, Ruvini</creatorcontrib><creatorcontrib>Youssef, Helmy Mohamad</creatorcontrib><creatorcontrib>Stein, Nils</creatorcontrib><creatorcontrib>Sreenivasulu, Nese</creatorcontrib><creatorcontrib>Komatsuda, Takao</creatorcontrib><creatorcontrib>Schnurbusch, Thorsten</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors 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>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Koppolu, Ravi</au><au>Anwar, Nadia</au><au>Sakuma, Shun</au><au>Tagiri, Akemi</au><au>Lundqvist, Udda</au><au>Pourkheirandish, Mohammad</au><au>Rutten, Twan</au><au>Seiler, Christiane</au><au>Himmelbach, Axel</au><au>Ariyadasa, Ruvini</au><au>Youssef, Helmy Mohamad</au><au>Stein, Nils</au><au>Sreenivasulu, Nese</au><au>Komatsuda, Takao</au><au>Schnurbusch, Thorsten</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Six-rowed spike4 (Vrs4) controls spikelet determinacy and row-type in barley</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2013-08-06</date><risdate>2013</risdate><volume>110</volume><issue>32</issue><spage>13198</spage><epage>13203</epage><pages>13198-13203</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Inflorescence architecture of barley (Hordeum vulgare L.) is common among the Triticeae species, which bear one to three singleflowered spikelets at each rachis internode. Triple spikelet meristem is one of the unique features of barley spikes, in which three spikelets (one central and two lateral spikelets) are produced at each rachis internode. Fertility of the lateral spikelets at triple spikelet meristem gives row-type identity to barley spikes. Sixrowed spikes show fertile lateral spikelets and produce increased grain yield per spike, compared with two-rowed spikes with sterile lateral spikelets. Thus, far, two loci governing the row-type phenotype were isolated in barley that include Six-rowed spikei (Vrs1) and Intermedium-C. In the present study, we isolated Six-rowed spike4 (Vrs4), a barley ortholog of the maize (Zea mays L.) inflorescence architecture gene RAMOSA2 (RA2). Eighteen coding mutations in barley RA2 (HvRA2) were specifically associated with lateral spikelet fertility and loss of spikelet determinacy. Expression analyses through mRNA in situ hybridization and microarray showed that Vrs4 (HvRA2) controls the row-type pathway through Vrs1 (HvHox1) a negative regulator of lateral spikelet fertility in barley. Moreover, Vrs4 may also regulate transcripts of barley SISTER OF RAMOSA3 (HvSRA), a putative trehalose-6-phosphate phosphatase involved in trehalose-6-phosphate homeostasis implicated to control spikelet determinacy. Our expression data illustrated that, although RA2 is conserved among different grass species, its down-stream target genes appear to be modified in barley and possibly other species of tribe Triticeae.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>23878219</pmid><doi>10.1073/pnas.1221950110</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Alleles Amino Acid Sequence Barley Base Sequence Biological Sciences Chromosome Mapping Chromosomes, Plant - genetics Corn Cytokinins Determinacy Fertility - genetics Gene expression Gene Expression Profiling Gene Expression Regulation, Plant Genes Genotype & phenotype grain yield grasses Haplotypes Homeostasis Hordeum - genetics Hordeum - metabolism Hordeum - ultrastructure Hordeum vulgare in situ hybridization Inflorescence - genetics Inflorescence - metabolism Inflorescence - ultrastructure Inflorescences loci Meristems messenger RNA microarray technology Microscopy, Electron, Scanning Molecular Sequence Data Mutation Nonnative species Oligonucleotide Array Sequence Analysis Phenotype Phenotypes Phylogeny Plant Proteins - classification Plant Proteins - genetics Plant Proteins - metabolism Reverse Transcriptase Polymerase Chain Reaction Sequence Homology, Amino Acid Spikelets Zea mays |
title | Six-rowed spike4 (Vrs4) controls spikelet determinacy and row-type in barley |
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