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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
Main Authors: Singh, Manjit, Kumar, Manish, Thilges, Katherine, Cho, Myeong-Je, Cigan, A Mark
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cited_by cdi_FETCH-LOGICAL-c593t-98d597488cdd967321beeb9be9b0d814911c1f07b033728652f80e396e033a7c3
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Kumar, Manish
Thilges, Katherine
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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.
doi_str_mv 10.1371/journal.pone.0177632
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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. 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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. 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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><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 - 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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 - 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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.</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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1932-6203
language eng
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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