empty pericarp4 Encodes a Mitochondrion-Targeted Pentatricopeptide Repeat Protein Necessary for Seed Development and Plant Growth in Maize
The pentatricopeptide repeat (PPR) family represents one of the largest gene families in plants, with >440 members annotated in Arabidopsis thaliana. PPR proteins are thought to have a major role in the regulation of posttranscriptional processes in organelles. Recent studies have shown that Arab...
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Veröffentlicht in: | The Plant cell 2007-01, Vol.19 (1), p.196-210 |
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creator | Gutiérrez-Marcos, José F Dal Prà, Mauro Giulini, Anna Costa, Liliana M Gavazzi, Giuseppe Cordelier, Sylvain Sellam, Olivier Tatout, Christophe Paul, Wyatt Perez, Pascual Dickinson, Hugh G Consonni, Gabriella |
description | The pentatricopeptide repeat (PPR) family represents one of the largest gene families in plants, with >440 members annotated in Arabidopsis thaliana. PPR proteins are thought to have a major role in the regulation of posttranscriptional processes in organelles. Recent studies have shown that Arabidopsis PPR proteins play an essential, nonredundant role during embryogenesis. Here, we demonstrate that mutations in empty pericarp4 (emp4), a maize (Zea mays) PPR-encoding gene, confer a seed-lethal phenotype. Mutant endosperms are severely impaired, with highly irregular differentiation of transfer cells in the nutrient-importing basal endosperm. Analysis of homozygous mutant plants generated from embryo-rescue experiments indicated that emp4 also affects general plant growth. The emp4-1 mutation was identified in an active Mutator (Mu) population, and cosegregation analysis revealed that it arose from a Mu3 element insertion. Evidence of emp4 molecular cloning was provided by the isolation of four additional emp4 alleles obtained by a reverse genetics approach. emp4 encodes a novel type of PPR protein of 614 amino acids. EMP4 contains nine 35-amino acid PPR motifs and an N-terminal mitochondrion-targeted sequence peptide, which was confirmed by a translational EMP4-green fluorescent protein fusion that localized to mitochondria. Molecular analyses further suggest that EMP4 is necessary to regulate the correct expression of a small subset of mitochondrial transcripts in the endosperm. |
doi_str_mv | 10.1105/tpc.105.039594 |
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PPR proteins are thought to have a major role in the regulation of posttranscriptional processes in organelles. Recent studies have shown that Arabidopsis PPR proteins play an essential, nonredundant role during embryogenesis. Here, we demonstrate that mutations in empty pericarp4 (emp4), a maize (Zea mays) PPR-encoding gene, confer a seed-lethal phenotype. Mutant endosperms are severely impaired, with highly irregular differentiation of transfer cells in the nutrient-importing basal endosperm. Analysis of homozygous mutant plants generated from embryo-rescue experiments indicated that emp4 also affects general plant growth. The emp4-1 mutation was identified in an active Mutator (Mu) population, and cosegregation analysis revealed that it arose from a Mu3 element insertion. Evidence of emp4 molecular cloning was provided by the isolation of four additional emp4 alleles obtained by a reverse genetics approach. emp4 encodes a novel type of PPR protein of 614 amino acids. EMP4 contains nine 35-amino acid PPR motifs and an N-terminal mitochondrion-targeted sequence peptide, which was confirmed by a translational EMP4-green fluorescent protein fusion that localized to mitochondria. Molecular analyses further suggest that EMP4 is necessary to regulate the correct expression of a small subset of mitochondrial transcripts in the endosperm.</description><identifier>ISSN: 1040-4651</identifier><identifier>ISSN: 1532-298X</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.105.039594</identifier><identifier>PMID: 17259266</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Amino Acid Motifs ; Amino acids ; Arabidopsis thaliana ; Cloning ; Cloning, Molecular ; Corn ; DNA ; Embryonic growth stage ; Embryos ; Endosperm ; Genetic mutation ; Genetics ; Green Fluorescent Proteins - analysis ; Life Sciences ; Mitochondria ; Mitochondria - metabolism ; Mitochondrial Proteins - genetics ; Mitochondrial Proteins - metabolism ; Molecular Sequence Data ; Multigene Family - physiology ; Mutation ; Phenotype ; Plant cells ; Plant growth ; Plant Proteins - chemistry ; Plant Proteins - genetics ; Plant Proteins - physiology ; Plants ; Plants genetics ; Proteins ; Recombinant Fusion Proteins - analysis ; RNA ; RNA, Messenger - metabolism ; Seeds - anatomy & histology ; Seeds - growth & development ; Seeds - metabolism ; Sequence Alignment ; Zea mays ; Zea mays - genetics ; Zea mays - growth & development ; Zea mays - metabolism</subject><ispartof>The Plant cell, 2007-01, Vol.19 (1), p.196-210</ispartof><rights>Copyright 2007 American Society of Plant Biologists</rights><rights>Copyright American Society of Plant Physiologists Jan 2007</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Copyright © 2007, American Society of Plant Biologists</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c518t-185a19e3e9b581cdf207b519b17d0483ef7dd061c1aea667800b09a19107faf13</citedby><cites>FETCH-LOGICAL-c518t-185a19e3e9b581cdf207b519b17d0483ef7dd061c1aea667800b09a19107faf13</cites><orcidid>0000-0002-3118-2762 ; 0000-0001-5215-2338</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/20076922$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/20076922$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,781,785,804,886,27929,27930,58022,58255</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17259266$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01927335$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Gutiérrez-Marcos, José F</creatorcontrib><creatorcontrib>Dal Prà, Mauro</creatorcontrib><creatorcontrib>Giulini, Anna</creatorcontrib><creatorcontrib>Costa, Liliana M</creatorcontrib><creatorcontrib>Gavazzi, Giuseppe</creatorcontrib><creatorcontrib>Cordelier, Sylvain</creatorcontrib><creatorcontrib>Sellam, Olivier</creatorcontrib><creatorcontrib>Tatout, Christophe</creatorcontrib><creatorcontrib>Paul, Wyatt</creatorcontrib><creatorcontrib>Perez, Pascual</creatorcontrib><creatorcontrib>Dickinson, Hugh G</creatorcontrib><creatorcontrib>Consonni, Gabriella</creatorcontrib><title>empty pericarp4 Encodes a Mitochondrion-Targeted Pentatricopeptide Repeat Protein Necessary for Seed Development and Plant Growth in Maize</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>The pentatricopeptide repeat (PPR) family represents one of the largest gene families in plants, with >440 members annotated in Arabidopsis thaliana. PPR proteins are thought to have a major role in the regulation of posttranscriptional processes in organelles. Recent studies have shown that Arabidopsis PPR proteins play an essential, nonredundant role during embryogenesis. Here, we demonstrate that mutations in empty pericarp4 (emp4), a maize (Zea mays) PPR-encoding gene, confer a seed-lethal phenotype. Mutant endosperms are severely impaired, with highly irregular differentiation of transfer cells in the nutrient-importing basal endosperm. Analysis of homozygous mutant plants generated from embryo-rescue experiments indicated that emp4 also affects general plant growth. The emp4-1 mutation was identified in an active Mutator (Mu) population, and cosegregation analysis revealed that it arose from a Mu3 element insertion. Evidence of emp4 molecular cloning was provided by the isolation of four additional emp4 alleles obtained by a reverse genetics approach. emp4 encodes a novel type of PPR protein of 614 amino acids. EMP4 contains nine 35-amino acid PPR motifs and an N-terminal mitochondrion-targeted sequence peptide, which was confirmed by a translational EMP4-green fluorescent protein fusion that localized to mitochondria. Molecular analyses further suggest that EMP4 is necessary to regulate the correct expression of a small subset of mitochondrial transcripts in the endosperm.</description><subject>Amino Acid Motifs</subject><subject>Amino acids</subject><subject>Arabidopsis thaliana</subject><subject>Cloning</subject><subject>Cloning, Molecular</subject><subject>Corn</subject><subject>DNA</subject><subject>Embryonic growth stage</subject><subject>Embryos</subject><subject>Endosperm</subject><subject>Genetic mutation</subject><subject>Genetics</subject><subject>Green Fluorescent Proteins - analysis</subject><subject>Life Sciences</subject><subject>Mitochondria</subject><subject>Mitochondria - metabolism</subject><subject>Mitochondrial Proteins - genetics</subject><subject>Mitochondrial Proteins - metabolism</subject><subject>Molecular Sequence Data</subject><subject>Multigene Family - physiology</subject><subject>Mutation</subject><subject>Phenotype</subject><subject>Plant cells</subject><subject>Plant growth</subject><subject>Plant Proteins - 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analysis</topic><topic>Life Sciences</topic><topic>Mitochondria</topic><topic>Mitochondria - metabolism</topic><topic>Mitochondrial Proteins - genetics</topic><topic>Mitochondrial Proteins - metabolism</topic><topic>Molecular Sequence Data</topic><topic>Multigene Family - physiology</topic><topic>Mutation</topic><topic>Phenotype</topic><topic>Plant cells</topic><topic>Plant growth</topic><topic>Plant Proteins - chemistry</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - physiology</topic><topic>Plants</topic><topic>Plants genetics</topic><topic>Proteins</topic><topic>Recombinant Fusion Proteins - analysis</topic><topic>RNA</topic><topic>RNA, Messenger - metabolism</topic><topic>Seeds - anatomy & histology</topic><topic>Seeds - growth & development</topic><topic>Seeds - metabolism</topic><topic>Sequence Alignment</topic><topic>Zea mays</topic><topic>Zea mays - genetics</topic><topic>Zea mays - growth & development</topic><topic>Zea mays - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gutiérrez-Marcos, José F</creatorcontrib><creatorcontrib>Dal Prà, Mauro</creatorcontrib><creatorcontrib>Giulini, Anna</creatorcontrib><creatorcontrib>Costa, Liliana M</creatorcontrib><creatorcontrib>Gavazzi, Giuseppe</creatorcontrib><creatorcontrib>Cordelier, Sylvain</creatorcontrib><creatorcontrib>Sellam, Olivier</creatorcontrib><creatorcontrib>Tatout, Christophe</creatorcontrib><creatorcontrib>Paul, Wyatt</creatorcontrib><creatorcontrib>Perez, Pascual</creatorcontrib><creatorcontrib>Dickinson, Hugh G</creatorcontrib><creatorcontrib>Consonni, Gabriella</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>ProQuest Central (Corporate)</collection><collection>Docstoc</collection><collection>Biotechnology Research Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>STEM Database</collection><collection>ProQuest Pharma Collection</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>Agricultural & Environmental Science Collection</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>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</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 Basic</collection><collection>Genetics Abstracts</collection><collection>SIRS Editorial</collection><collection>MEDLINE - 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PPR proteins are thought to have a major role in the regulation of posttranscriptional processes in organelles. Recent studies have shown that Arabidopsis PPR proteins play an essential, nonredundant role during embryogenesis. Here, we demonstrate that mutations in empty pericarp4 (emp4), a maize (Zea mays) PPR-encoding gene, confer a seed-lethal phenotype. Mutant endosperms are severely impaired, with highly irregular differentiation of transfer cells in the nutrient-importing basal endosperm. Analysis of homozygous mutant plants generated from embryo-rescue experiments indicated that emp4 also affects general plant growth. The emp4-1 mutation was identified in an active Mutator (Mu) population, and cosegregation analysis revealed that it arose from a Mu3 element insertion. Evidence of emp4 molecular cloning was provided by the isolation of four additional emp4 alleles obtained by a reverse genetics approach. emp4 encodes a novel type of PPR protein of 614 amino acids. EMP4 contains nine 35-amino acid PPR motifs and an N-terminal mitochondrion-targeted sequence peptide, which was confirmed by a translational EMP4-green fluorescent protein fusion that localized to mitochondria. Molecular analyses further suggest that EMP4 is necessary to regulate the correct expression of a small subset of mitochondrial transcripts in the endosperm.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>17259266</pmid><doi>10.1105/tpc.105.039594</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-3118-2762</orcidid><orcidid>https://orcid.org/0000-0001-5215-2338</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amino Acid Motifs Amino acids Arabidopsis thaliana Cloning Cloning, Molecular Corn DNA Embryonic growth stage Embryos Endosperm Genetic mutation Genetics Green Fluorescent Proteins - analysis Life Sciences Mitochondria Mitochondria - metabolism Mitochondrial Proteins - genetics Mitochondrial Proteins - metabolism Molecular Sequence Data Multigene Family - physiology Mutation Phenotype Plant cells Plant growth Plant Proteins - chemistry Plant Proteins - genetics Plant Proteins - physiology Plants Plants genetics Proteins Recombinant Fusion Proteins - analysis RNA RNA, Messenger - metabolism Seeds - anatomy & histology Seeds - growth & development Seeds - metabolism Sequence Alignment Zea mays Zea mays - genetics Zea mays - growth & development Zea mays - metabolism |
title | empty pericarp4 Encodes a Mitochondrion-Targeted Pentatricopeptide Repeat Protein Necessary for Seed Development and Plant Growth in Maize |
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