Transgenic Pm3b wheat lines show resistance to powdery mildew in the field

Summary Plant resistance (R) genes are highly effective in protecting plants against diseases, but pathogens can overcome such genes relatively easily by adaptation. Consequently, in many cases R genes do not confer durable resistance in agricultural environments. One possible strategy to make the u...

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Veröffentlicht in:Plant biotechnology journal 2011-10, Vol.9 (8), p.897-910
Hauptverfasser: Brunner, Susanne, Hurni, Severine, Herren, Gerhard, Kalinina, Olena, von Burg, Simone, Zeller, Simon L., Schmid, Bernhard, Winzeler, Michael, Keller, Beat
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container_title Plant biotechnology journal
container_volume 9
creator Brunner, Susanne
Hurni, Severine
Herren, Gerhard
Kalinina, Olena
von Burg, Simone
Zeller, Simon L.
Schmid, Bernhard
Winzeler, Michael
Keller, Beat
description Summary Plant resistance (R) genes are highly effective in protecting plants against diseases, but pathogens can overcome such genes relatively easily by adaptation. Consequently, in many cases R genes do not confer durable resistance in agricultural environments. One possible strategy to make the use of R genes more sustainable depends on the modification of R genes followed by transformation. To test a possible transgenic use of R genes, we overexpressed in wheat the Pm3b resistance gene against powdery mildew under control of the maize ubiquitin promoter. Four independent transgenic lines were tested in the greenhouse and the field during 3 years. The four lines showed a five‐ to 600‐fold transgene overexpression compared with the expression of the endogenous Pm3b gene in the landrace ‘Chul’. Powdery mildew resistance was significantly improved in all lines in the greenhouse and the field, both with naturally occurring infection or after artificial inoculation. Under controlled environmental conditions, the line with the strongest overexpression of the Pm3b gene showed a dramatic increase in resistance to powdery mildew isolates that are virulent on the endogenous Pm3b. Under a variety of field conditions, but never in the greenhouse, three of the four transgenic lines showed pleiotropic effects on spike and leaf morphology. The highest overexpressing line had the strongest side effects, suggesting a correlation between expression level and phenotypic changes. These results demonstrate that the successful transgenic use of R genes critically depends on achieving an optimal level of their expression, possibly in a tissue‐specific way.
doi_str_mv 10.1111/j.1467-7652.2011.00603.x
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Consequently, in many cases R genes do not confer durable resistance in agricultural environments. One possible strategy to make the use of R genes more sustainable depends on the modification of R genes followed by transformation. To test a possible transgenic use of R genes, we overexpressed in wheat the Pm3b resistance gene against powdery mildew under control of the maize ubiquitin promoter. Four independent transgenic lines were tested in the greenhouse and the field during 3 years. The four lines showed a five‐ to 600‐fold transgene overexpression compared with the expression of the endogenous Pm3b gene in the landrace ‘Chul’. Powdery mildew resistance was significantly improved in all lines in the greenhouse and the field, both with naturally occurring infection or after artificial inoculation. Under controlled environmental conditions, the line with the strongest overexpression of the Pm3b gene showed a dramatic increase in resistance to powdery mildew isolates that are virulent on the endogenous Pm3b. Under a variety of field conditions, but never in the greenhouse, three of the four transgenic lines showed pleiotropic effects on spike and leaf morphology. The highest overexpressing line had the strongest side effects, suggesting a correlation between expression level and phenotypic changes. These results demonstrate that the successful transgenic use of R genes critically depends on achieving an optimal level of their expression, possibly in a tissue‐specific way.</description><identifier>ISSN: 1467-7644</identifier><identifier>EISSN: 1467-7652</identifier><identifier>DOI: 10.1111/j.1467-7652.2011.00603.x</identifier><identifier>PMID: 21438988</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Ascomycota - drug effects ; Ascomycota - pathogenicity ; Biological and medical sciences ; Biotechnology ; Cloning, Molecular ; Disease Resistance ; field trial ; Flowers - metabolism ; Fundamental and applied biological sciences. Psychology ; Fungicides, Industrial - pharmacology ; Gene Expression Regulation, Plant ; Gene Silencing ; Genetic Pleiotropy ; Genetic Vectors - genetics ; Genotype ; GMO ; Mannose-6-Phosphate Isomerase - genetics ; Mannose-6-Phosphate Isomerase - metabolism ; Plant Diseases - immunology ; Plant Diseases - microbiology ; Plant Leaves - growth &amp; development ; Plant Leaves - metabolism ; Plant Leaves - microbiology ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant Stems - growth &amp; development ; Plant Stems - metabolism ; Plants, Genetically Modified - genetics ; Plants, Genetically Modified - immunology ; Plants, Genetically Modified - metabolism ; Plants, Genetically Modified - microbiology ; Pm3b ; powdery mildew ; Promoter Regions, Genetic ; R gene overexpression ; Transgenes ; Triticum - genetics ; Triticum - immunology ; Triticum - metabolism ; Triticum - microbiology ; wheat</subject><ispartof>Plant biotechnology journal, 2011-10, Vol.9 (8), p.897-910</ispartof><rights>2011 The Authors. Plant Biotechnology Journal © 2011 Society for Experimental Biology, Association of Applied Biologists and Blackwell Publishing Ltd</rights><rights>2015 INIST-CNRS</rights><rights>2011 The Authors. 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Consequently, in many cases R genes do not confer durable resistance in agricultural environments. One possible strategy to make the use of R genes more sustainable depends on the modification of R genes followed by transformation. To test a possible transgenic use of R genes, we overexpressed in wheat the Pm3b resistance gene against powdery mildew under control of the maize ubiquitin promoter. Four independent transgenic lines were tested in the greenhouse and the field during 3 years. The four lines showed a five‐ to 600‐fold transgene overexpression compared with the expression of the endogenous Pm3b gene in the landrace ‘Chul’. Powdery mildew resistance was significantly improved in all lines in the greenhouse and the field, both with naturally occurring infection or after artificial inoculation. Under controlled environmental conditions, the line with the strongest overexpression of the Pm3b gene showed a dramatic increase in resistance to powdery mildew isolates that are virulent on the endogenous Pm3b. Under a variety of field conditions, but never in the greenhouse, three of the four transgenic lines showed pleiotropic effects on spike and leaf morphology. The highest overexpressing line had the strongest side effects, suggesting a correlation between expression level and phenotypic changes. These results demonstrate that the successful transgenic use of R genes critically depends on achieving an optimal level of their expression, possibly in a tissue‐specific way.</description><subject>Ascomycota - drug effects</subject><subject>Ascomycota - pathogenicity</subject><subject>Biological and medical sciences</subject><subject>Biotechnology</subject><subject>Cloning, Molecular</subject><subject>Disease Resistance</subject><subject>field trial</subject><subject>Flowers - metabolism</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Fungicides, Industrial - pharmacology</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Silencing</subject><subject>Genetic Pleiotropy</subject><subject>Genetic Vectors - genetics</subject><subject>Genotype</subject><subject>GMO</subject><subject>Mannose-6-Phosphate Isomerase - genetics</subject><subject>Mannose-6-Phosphate Isomerase - metabolism</subject><subject>Plant Diseases - immunology</subject><subject>Plant Diseases - microbiology</subject><subject>Plant Leaves - growth &amp; development</subject><subject>Plant Leaves - metabolism</subject><subject>Plant Leaves - microbiology</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Stems - growth &amp; development</subject><subject>Plant Stems - metabolism</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Plants, Genetically Modified - immunology</subject><subject>Plants, Genetically Modified - metabolism</subject><subject>Plants, Genetically Modified - microbiology</subject><subject>Pm3b</subject><subject>powdery mildew</subject><subject>Promoter Regions, Genetic</subject><subject>R gene overexpression</subject><subject>Transgenes</subject><subject>Triticum - genetics</subject><subject>Triticum - immunology</subject><subject>Triticum - metabolism</subject><subject>Triticum - microbiology</subject><subject>wheat</subject><issn>1467-7644</issn><issn>1467-7652</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUtv1DAURi1UREvhL1TeoK4S_LYjsaFVKUUVLVBaqRvL49wwHvIY7Iwy8-9JOsOw7d3Yls93bR8jhCnJ6VjvFzkVSmdaSZYzQmlOiCI8X79AR_uNg_1ciEP0OqUFIYwqqV6hQ0YFN4UxR-jLXXRt-gVt8Pi24TM8zMH1uA4tJJzm3YAjpJB613rAfYeX3VBC3OAm1CUMOLS4nwOuAtTlG_SycnWCt7vxGP38dHF3_jm7vrm8Ov94nXlhJM-YkZVkZaEY9VA6XzijtWOgnR6LSUG8kpUrgUpu9EzwqmClN64al8QL4MfodNt3Gbs_K0i9bULyUNeuhW6VrDGGFIQSPpJmS_rYpRShsssYGhc3lhI7ibQLOzmyky87ibRPIu16jJ7sDlnNGij3wX_mRuDdDnDJu7oaNfqQ_nNCSlLwifuw5YZQw-bZF7C3Z1fq6QnZNj7-Aaz3cRd_W6W5lvbh66Wl6tvZD37_3T7yv-fcnKg</recordid><startdate>201110</startdate><enddate>201110</enddate><creator>Brunner, Susanne</creator><creator>Hurni, Severine</creator><creator>Herren, Gerhard</creator><creator>Kalinina, Olena</creator><creator>von Burg, Simone</creator><creator>Zeller, Simon L.</creator><creator>Schmid, Bernhard</creator><creator>Winzeler, Michael</creator><creator>Keller, Beat</creator><general>Blackwell Publishing Ltd</general><general>Blackwell</general><scope>BSCLL</scope><scope>IQODW</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></search><sort><creationdate>201110</creationdate><title>Transgenic Pm3b wheat lines show resistance to powdery mildew in the field</title><author>Brunner, Susanne ; Hurni, Severine ; Herren, Gerhard ; Kalinina, Olena ; von Burg, Simone ; Zeller, Simon L. ; Schmid, Bernhard ; Winzeler, Michael ; Keller, Beat</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4853-285f52d9621cedac9a877a2e7a77772540c65fade15387b43f92dc8af5380c4e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Ascomycota - drug effects</topic><topic>Ascomycota - pathogenicity</topic><topic>Biological and medical sciences</topic><topic>Biotechnology</topic><topic>Cloning, Molecular</topic><topic>Disease Resistance</topic><topic>field trial</topic><topic>Flowers - metabolism</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Fungicides, Industrial - pharmacology</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene Silencing</topic><topic>Genetic Pleiotropy</topic><topic>Genetic Vectors - genetics</topic><topic>Genotype</topic><topic>GMO</topic><topic>Mannose-6-Phosphate Isomerase - genetics</topic><topic>Mannose-6-Phosphate Isomerase - metabolism</topic><topic>Plant Diseases - immunology</topic><topic>Plant Diseases - microbiology</topic><topic>Plant Leaves - growth &amp; development</topic><topic>Plant Leaves - metabolism</topic><topic>Plant Leaves - microbiology</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Stems - growth &amp; development</topic><topic>Plant Stems - metabolism</topic><topic>Plants, Genetically Modified - genetics</topic><topic>Plants, Genetically Modified - immunology</topic><topic>Plants, Genetically Modified - metabolism</topic><topic>Plants, Genetically Modified - microbiology</topic><topic>Pm3b</topic><topic>powdery mildew</topic><topic>Promoter Regions, Genetic</topic><topic>R gene overexpression</topic><topic>Transgenes</topic><topic>Triticum - genetics</topic><topic>Triticum - immunology</topic><topic>Triticum - metabolism</topic><topic>Triticum - microbiology</topic><topic>wheat</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brunner, Susanne</creatorcontrib><creatorcontrib>Hurni, Severine</creatorcontrib><creatorcontrib>Herren, Gerhard</creatorcontrib><creatorcontrib>Kalinina, Olena</creatorcontrib><creatorcontrib>von Burg, Simone</creatorcontrib><creatorcontrib>Zeller, Simon L.</creatorcontrib><creatorcontrib>Schmid, Bernhard</creatorcontrib><creatorcontrib>Winzeler, Michael</creatorcontrib><creatorcontrib>Keller, Beat</creatorcontrib><collection>Istex</collection><collection>Pascal-Francis</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><jtitle>Plant biotechnology journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext_linktorsrc</fulltext></delivery><addata><au>Brunner, Susanne</au><au>Hurni, Severine</au><au>Herren, Gerhard</au><au>Kalinina, Olena</au><au>von Burg, Simone</au><au>Zeller, Simon L.</au><au>Schmid, Bernhard</au><au>Winzeler, Michael</au><au>Keller, Beat</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Transgenic Pm3b wheat lines show resistance to powdery mildew in the field</atitle><jtitle>Plant biotechnology journal</jtitle><addtitle>Plant Biotechnol J</addtitle><date>2011-10</date><risdate>2011</risdate><volume>9</volume><issue>8</issue><spage>897</spage><epage>910</epage><pages>897-910</pages><issn>1467-7644</issn><eissn>1467-7652</eissn><abstract>Summary Plant resistance (R) genes are highly effective in protecting plants against diseases, but pathogens can overcome such genes relatively easily by adaptation. Consequently, in many cases R genes do not confer durable resistance in agricultural environments. One possible strategy to make the use of R genes more sustainable depends on the modification of R genes followed by transformation. To test a possible transgenic use of R genes, we overexpressed in wheat the Pm3b resistance gene against powdery mildew under control of the maize ubiquitin promoter. Four independent transgenic lines were tested in the greenhouse and the field during 3 years. The four lines showed a five‐ to 600‐fold transgene overexpression compared with the expression of the endogenous Pm3b gene in the landrace ‘Chul’. Powdery mildew resistance was significantly improved in all lines in the greenhouse and the field, both with naturally occurring infection or after artificial inoculation. Under controlled environmental conditions, the line with the strongest overexpression of the Pm3b gene showed a dramatic increase in resistance to powdery mildew isolates that are virulent on the endogenous Pm3b. Under a variety of field conditions, but never in the greenhouse, three of the four transgenic lines showed pleiotropic effects on spike and leaf morphology. The highest overexpressing line had the strongest side effects, suggesting a correlation between expression level and phenotypic changes. These results demonstrate that the successful transgenic use of R genes critically depends on achieving an optimal level of their expression, possibly in a tissue‐specific way.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>21438988</pmid><doi>10.1111/j.1467-7652.2011.00603.x</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record>
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source Wiley Online Library Open Access
subjects Ascomycota - drug effects
Ascomycota - pathogenicity
Biological and medical sciences
Biotechnology
Cloning, Molecular
Disease Resistance
field trial
Flowers - metabolism
Fundamental and applied biological sciences. Psychology
Fungicides, Industrial - pharmacology
Gene Expression Regulation, Plant
Gene Silencing
Genetic Pleiotropy
Genetic Vectors - genetics
Genotype
GMO
Mannose-6-Phosphate Isomerase - genetics
Mannose-6-Phosphate Isomerase - metabolism
Plant Diseases - immunology
Plant Diseases - microbiology
Plant Leaves - growth & development
Plant Leaves - metabolism
Plant Leaves - microbiology
Plant Proteins - genetics
Plant Proteins - metabolism
Plant Stems - growth & development
Plant Stems - metabolism
Plants, Genetically Modified - genetics
Plants, Genetically Modified - immunology
Plants, Genetically Modified - metabolism
Plants, Genetically Modified - microbiology
Pm3b
powdery mildew
Promoter Regions, Genetic
R gene overexpression
Transgenes
Triticum - genetics
Triticum - immunology
Triticum - metabolism
Triticum - microbiology
wheat
title Transgenic Pm3b wheat lines show resistance to powdery mildew in the field
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