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MS26/CYP704B is required for anther and pollen wall development in bread wheat (Triticum aestivum L.) and combining mutations in all three homeologs causes male sterility
Development of anthers and pollen represents an important aspect of the life cycle in flowering plants. Genes contributing to anther and pollen development have been widely studied in many plant species. Ms26/CYP704B genes play an important role in pollen development through biosynthesis of sporopol...
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Published in: | PloS one 2017-05, Vol.12 (5), p.e0177632-e0177632 |
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description | Development of anthers and pollen represents an important aspect of the life cycle in flowering plants. Genes contributing to anther and pollen development have been widely studied in many plant species. Ms26/CYP704B genes play an important role in pollen development through biosynthesis of sporopollenin for pollen exine formation. To investigate the role of Ms26/CYP704B genes in anther and pollen development of bread wheat, mutations in the A-, B-, and D-homeologs of the putative Ms26/CYP704B gene were analyzed. Single and double homozygous mutants in any of the homeologs did not affect pollen development and male fertility. Triple homozygous mutants resulted in completely male sterile plants that were defective in pollen and anther development. Additionally, double homozygous-single heterozygous mutants were also male sterile although with varying levels of residual fertility. The fertility of these triple mutants was dependent upon the homeolog contributing the wild-type allele. Two heterologous Ms26/CYP704B genes, when transformed into a triple homozygous mutant background, completely restored male fertility, whereas a single gene was unable to restore fertility. Functional analysis of Ms26/CYP704B furthers the understanding of male fertility genes which can be utilized for the development of novel hybrid seed production systems in wheat. |
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Genes contributing to anther and pollen development have been widely studied in many plant species. Ms26/CYP704B genes play an important role in pollen development through biosynthesis of sporopollenin for pollen exine formation. To investigate the role of Ms26/CYP704B genes in anther and pollen development of bread wheat, mutations in the A-, B-, and D-homeologs of the putative Ms26/CYP704B gene were analyzed. Single and double homozygous mutants in any of the homeologs did not affect pollen development and male fertility. Triple homozygous mutants resulted in completely male sterile plants that were defective in pollen and anther development. Additionally, double homozygous-single heterozygous mutants were also male sterile although with varying levels of residual fertility. The fertility of these triple mutants was dependent upon the homeolog contributing the wild-type allele. Two heterologous Ms26/CYP704B genes, when transformed into a triple homozygous mutant background, completely restored male fertility, whereas a single gene was unable to restore fertility. Functional analysis of Ms26/CYP704B furthers the understanding of male fertility genes which can be utilized for the development of novel hybrid seed production systems in wheat.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0177632</identifier><identifier>PMID: 28520767</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Airborne microorganisms ; Alignment ; Alleles ; Amino Acid Sequence ; Amino acids ; Anthers ; Assembly ; Asymmetry ; BAK protein ; Barley ; Biochemical analysis ; Biochemistry ; Biological evolution ; Biology and Life Sciences ; Biosynthesis ; Blast ; Cellulose ; Chalcone synthase ; Cloning ; Corn ; Crops ; Cytochrome ; Cytochrome P-450 Enzyme System - chemistry ; Cytochrome P-450 Enzyme System - genetics ; Cytochrome P-450 Enzyme System - metabolism ; Defects ; Deoxyribonucleic acid ; Deposition ; DNA ; Environmental conditions ; Enzymes ; Epigenetics ; Evolution ; Exons ; Exploitation ; Fatty acids ; Fertility ; Fertilization ; Flowers - genetics ; Functional analysis ; Fungi ; Gametes ; Gene expression ; Gene Expression Regulation, Plant ; Gene mapping ; Genes, Recessive ; Genetic aspects ; Genetic Complementation Test ; Genetics ; Genomes ; Genomics ; Goat grass ; Grain ; Grasses ; Homing ; Homology ; Male sterility ; Mutagenesis ; Mutants ; Mutation ; Nucleotide sequence ; Organs ; Plant cuticle ; Plant fertilization ; Plant genetics ; Plant Infertility - genetics ; Plant Proteins - chemistry ; Plant Proteins - genetics ; Pollen ; Pollen - genetics ; Polyploidy ; Proteins ; Reproductive organs ; Research and Analysis Methods ; Sorghum ; Stem cells ; Synteny ; Triticum - physiology ; Triticum aestivum ; Wheat</subject><ispartof>PloS one, 2017-05, Vol.12 (5), p.e0177632-e0177632</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Singh et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2017 Singh et al 2017 Singh et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c593t-98d597488cdd967321beeb9be9b0d814911c1f07b033728652f80e396e033a7c3</citedby><cites>FETCH-LOGICAL-c593t-98d597488cdd967321beeb9be9b0d814911c1f07b033728652f80e396e033a7c3</cites><orcidid>0000-0002-7638-7235 ; 0000-0001-7706-9418</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1899376050/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1899376050?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25752,27923,27924,37011,37012,44589,53790,53792,74897</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28520767$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Sandhu, Devinder</contributor><creatorcontrib>Singh, Manjit</creatorcontrib><creatorcontrib>Kumar, Manish</creatorcontrib><creatorcontrib>Thilges, Katherine</creatorcontrib><creatorcontrib>Cho, Myeong-Je</creatorcontrib><creatorcontrib>Cigan, A Mark</creatorcontrib><title>MS26/CYP704B is required for anther and pollen wall development in bread wheat (Triticum aestivum L.) and combining mutations in all three homeologs causes male sterility</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Development of anthers and pollen represents an important aspect of the life cycle in flowering plants. Genes contributing to anther and pollen development have been widely studied in many plant species. Ms26/CYP704B genes play an important role in pollen development through biosynthesis of sporopollenin for pollen exine formation. To investigate the role of Ms26/CYP704B genes in anther and pollen development of bread wheat, mutations in the A-, B-, and D-homeologs of the putative Ms26/CYP704B gene were analyzed. Single and double homozygous mutants in any of the homeologs did not affect pollen development and male fertility. Triple homozygous mutants resulted in completely male sterile plants that were defective in pollen and anther development. Additionally, double homozygous-single heterozygous mutants were also male sterile although with varying levels of residual fertility. The fertility of these triple mutants was dependent upon the homeolog contributing the wild-type allele. Two heterologous Ms26/CYP704B genes, when transformed into a triple homozygous mutant background, completely restored male fertility, whereas a single gene was unable to restore fertility. Functional analysis of Ms26/CYP704B furthers the understanding of male fertility genes which can be utilized for the development of novel hybrid seed production systems in wheat.</description><subject>Airborne microorganisms</subject><subject>Alignment</subject><subject>Alleles</subject><subject>Amino Acid Sequence</subject><subject>Amino acids</subject><subject>Anthers</subject><subject>Assembly</subject><subject>Asymmetry</subject><subject>BAK protein</subject><subject>Barley</subject><subject>Biochemical analysis</subject><subject>Biochemistry</subject><subject>Biological evolution</subject><subject>Biology and Life Sciences</subject><subject>Biosynthesis</subject><subject>Blast</subject><subject>Cellulose</subject><subject>Chalcone synthase</subject><subject>Cloning</subject><subject>Corn</subject><subject>Crops</subject><subject>Cytochrome</subject><subject>Cytochrome P-450 Enzyme System - chemistry</subject><subject>Cytochrome P-450 Enzyme System - genetics</subject><subject>Cytochrome P-450 Enzyme System - metabolism</subject><subject>Defects</subject><subject>Deoxyribonucleic acid</subject><subject>Deposition</subject><subject>DNA</subject><subject>Environmental conditions</subject><subject>Enzymes</subject><subject>Epigenetics</subject><subject>Evolution</subject><subject>Exons</subject><subject>Exploitation</subject><subject>Fatty acids</subject><subject>Fertility</subject><subject>Fertilization</subject><subject>Flowers - genetics</subject><subject>Functional analysis</subject><subject>Fungi</subject><subject>Gametes</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene mapping</subject><subject>Genes, Recessive</subject><subject>Genetic aspects</subject><subject>Genetic Complementation Test</subject><subject>Genetics</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Goat grass</subject><subject>Grain</subject><subject>Grasses</subject><subject>Homing</subject><subject>Homology</subject><subject>Male sterility</subject><subject>Mutagenesis</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Nucleotide sequence</subject><subject>Organs</subject><subject>Plant cuticle</subject><subject>Plant fertilization</subject><subject>Plant genetics</subject><subject>Plant Infertility - genetics</subject><subject>Plant Proteins - chemistry</subject><subject>Plant Proteins - genetics</subject><subject>Pollen</subject><subject>Pollen - genetics</subject><subject>Polyploidy</subject><subject>Proteins</subject><subject>Reproductive organs</subject><subject>Research and Analysis Methods</subject><subject>Sorghum</subject><subject>Stem cells</subject><subject>Synteny</subject><subject>Triticum - physiology</subject><subject>Triticum aestivum</subject><subject>Wheat</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptks1u1DAUhSMEomXgDRBYYlMWM_VPEtubSmXET6VBIFEWrCzHuZlx5cRTO5mqr8RT4nTSqoMqL2xdn_v5-uhk2VuCF4Rxcnrlh9Bpt9j6DhaYcF4y-iw7JpLReUkxe_7ofJS9ivEK44KJsnyZHVFRUMxLfpz9_f6LlqfLPz85zj8hG1GA68EGqFHjA9Jdv4Fxq9HWOwcdutHOoRp24Py2ha5HtkNVAF2jmw3oHp1cBttbM7RIQ-ztLh1Wi493BOPbyna2W6N26HVvfRfH7hHYbwIA2vgWvPPriIweIkTUagco9hCss_3t6-xFo12EN9M-y35_-Xy5_DZf_fh6sTxfzU0hWT-Xoi4kz4UwdS1LziipACpZgaxwLUguCTGkwbzCjHEqyoI2AgOTJaSC5obNsvd77tb5qCaboyJCSsZLXOCkuNgraq-v1DbYVodb5bVVdwUf1kqH5IIDRTTTGhe8kRrnuAAJuKbM4FxgUWkqE-tsem2oWqhN8jRodwA9vOnsRq39ThX5OD9NgJMJEPz1kExXrY0GnNMd-CHNLTEWTBRilH74T_r07ybVOtmvbNf49K4Zoeo8uZc4PAFn2eIJVVo1tNakTDY21Q8a8n2DCT7GAM3DHwlWY6Lvh1FjotWU6NT27rE_D033EWb_AC-y844</recordid><startdate>20170516</startdate><enddate>20170516</enddate><creator>Singh, Manjit</creator><creator>Kumar, Manish</creator><creator>Thilges, Katherine</creator><creator>Cho, Myeong-Je</creator><creator>Cigan, A Mark</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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</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>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-7638-7235</orcidid><orcidid>https://orcid.org/0000-0001-7706-9418</orcidid></search><sort><creationdate>20170516</creationdate><title>MS26/CYP704B is required for anther and pollen wall development in bread wheat (Triticum aestivum L.) and combining mutations in all three homeologs causes male sterility</title><author>Singh, Manjit ; Kumar, Manish ; Thilges, Katherine ; Cho, Myeong-Je ; Cigan, A Mark</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c593t-98d597488cdd967321beeb9be9b0d814911c1f07b033728652f80e396e033a7c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Airborne microorganisms</topic><topic>Alignment</topic><topic>Alleles</topic><topic>Amino Acid Sequence</topic><topic>Amino acids</topic><topic>Anthers</topic><topic>Assembly</topic><topic>Asymmetry</topic><topic>BAK protein</topic><topic>Barley</topic><topic>Biochemical analysis</topic><topic>Biochemistry</topic><topic>Biological evolution</topic><topic>Biology and Life Sciences</topic><topic>Biosynthesis</topic><topic>Blast</topic><topic>Cellulose</topic><topic>Chalcone synthase</topic><topic>Cloning</topic><topic>Corn</topic><topic>Crops</topic><topic>Cytochrome</topic><topic>Cytochrome P-450 Enzyme System - chemistry</topic><topic>Cytochrome P-450 Enzyme System - genetics</topic><topic>Cytochrome P-450 Enzyme System - metabolism</topic><topic>Defects</topic><topic>Deoxyribonucleic acid</topic><topic>Deposition</topic><topic>DNA</topic><topic>Environmental conditions</topic><topic>Enzymes</topic><topic>Epigenetics</topic><topic>Evolution</topic><topic>Exons</topic><topic>Exploitation</topic><topic>Fatty acids</topic><topic>Fertility</topic><topic>Fertilization</topic><topic>Flowers - genetics</topic><topic>Functional analysis</topic><topic>Fungi</topic><topic>Gametes</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene mapping</topic><topic>Genes, Recessive</topic><topic>Genetic aspects</topic><topic>Genetic Complementation Test</topic><topic>Genetics</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Goat grass</topic><topic>Grain</topic><topic>Grasses</topic><topic>Homing</topic><topic>Homology</topic><topic>Male sterility</topic><topic>Mutagenesis</topic><topic>Mutants</topic><topic>Mutation</topic><topic>Nucleotide sequence</topic><topic>Organs</topic><topic>Plant cuticle</topic><topic>Plant fertilization</topic><topic>Plant genetics</topic><topic>Plant Infertility - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Singh, Manjit</au><au>Kumar, Manish</au><au>Thilges, Katherine</au><au>Cho, Myeong-Je</au><au>Cigan, A Mark</au><au>Sandhu, Devinder</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>MS26/CYP704B is required for anther and pollen wall development in bread wheat (Triticum aestivum L.) and combining mutations in all three homeologs causes male sterility</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-05-16</date><risdate>2017</risdate><volume>12</volume><issue>5</issue><spage>e0177632</spage><epage>e0177632</epage><pages>e0177632-e0177632</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Development of anthers and pollen represents an important aspect of the life cycle in flowering plants. Genes contributing to anther and pollen development have been widely studied in many plant species. Ms26/CYP704B genes play an important role in pollen development through biosynthesis of sporopollenin for pollen exine formation. To investigate the role of Ms26/CYP704B genes in anther and pollen development of bread wheat, mutations in the A-, B-, and D-homeologs of the putative Ms26/CYP704B gene were analyzed. Single and double homozygous mutants in any of the homeologs did not affect pollen development and male fertility. Triple homozygous mutants resulted in completely male sterile plants that were defective in pollen and anther development. Additionally, double homozygous-single heterozygous mutants were also male sterile although with varying levels of residual fertility. The fertility of these triple mutants was dependent upon the homeolog contributing the wild-type allele. Two heterologous Ms26/CYP704B genes, when transformed into a triple homozygous mutant background, completely restored male fertility, whereas a single gene was unable to restore fertility. Functional analysis of Ms26/CYP704B furthers the understanding of male fertility genes which can be utilized for the development of novel hybrid seed production systems in wheat.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28520767</pmid><doi>10.1371/journal.pone.0177632</doi><orcidid>https://orcid.org/0000-0002-7638-7235</orcidid><orcidid>https://orcid.org/0000-0001-7706-9418</orcidid><oa>free_for_read</oa></addata></record> |
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source | PubMed (Medline); Publicly Available Content Database |
subjects | Airborne microorganisms Alignment Alleles Amino Acid Sequence Amino acids Anthers Assembly Asymmetry BAK protein Barley Biochemical analysis Biochemistry Biological evolution Biology and Life Sciences Biosynthesis Blast Cellulose Chalcone synthase Cloning Corn Crops Cytochrome Cytochrome P-450 Enzyme System - chemistry Cytochrome P-450 Enzyme System - genetics Cytochrome P-450 Enzyme System - metabolism Defects Deoxyribonucleic acid Deposition DNA Environmental conditions Enzymes Epigenetics Evolution Exons Exploitation Fatty acids Fertility Fertilization Flowers - genetics Functional analysis Fungi Gametes Gene expression Gene Expression Regulation, Plant Gene mapping Genes, Recessive Genetic aspects Genetic Complementation Test Genetics Genomes Genomics Goat grass Grain Grasses Homing Homology Male sterility Mutagenesis Mutants Mutation Nucleotide sequence Organs Plant cuticle Plant fertilization Plant genetics Plant Infertility - genetics Plant Proteins - chemistry Plant Proteins - genetics Pollen Pollen - genetics Polyploidy Proteins Reproductive organs Research and Analysis Methods Sorghum Stem cells Synteny Triticum - physiology Triticum aestivum Wheat |
title | MS26/CYP704B is required for anther and pollen wall development in bread wheat (Triticum aestivum L.) and combining mutations in all three homeologs causes male sterility |
url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-11T18%3A57%3A03IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=MS26/CYP704B%20is%20required%20for%20anther%20and%20pollen%20wall%20development%20in%20bread%20wheat%20(Triticum%20aestivum%20L.)%20and%20combining%20mutations%20in%20all%20three%20homeologs%20causes%20male%20sterility&rft.jtitle=PloS%20one&rft.au=Singh,%20Manjit&rft.date=2017-05-16&rft.volume=12&rft.issue=5&rft.spage=e0177632&rft.epage=e0177632&rft.pages=e0177632-e0177632&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0177632&rft_dat=%3Cgale_plos_%3EA491823708%3C/gale_plos_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c593t-98d597488cdd967321beeb9be9b0d814911c1f07b033728652f80e396e033a7c3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=1899376050&rft_id=info:pmid/28520767&rft_galeid=A491823708&rfr_iscdi=true |