The Tomato Yellow Leaf Curl Virus Resistance Genes Ty-1 and Ty-3 Are Allelic and Code for DFDGD-Class RNA–Dependent RNA Polymerases

Tomato Yellow Leaf Curl Virus Disease incited by Tomato yellow leaf curl virus (TYLCV) causes huge losses in tomato production worldwide and is caused by different related begomovirus species. Breeding for TYLCV resistance has been based on the introgression of multiple resistance genes originating...

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Vydáno v:PLoS genetics Ročník 9; číslo 3; s. e1003399
Hlavní autoři: Verlaan, Maarten G., Hutton, Samuel F., Ibrahem, Ragy M., Kormelink, Richard, Visser, Richard G. F., Scott, John W., Edwards, Jeremy D., Bai, Yuling
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States Public Library of Science 01.03.2013
Public Library of Science (PLoS)
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ISSN:1553-7404, 1553-7390, 1553-7404
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Abstract Tomato Yellow Leaf Curl Virus Disease incited by Tomato yellow leaf curl virus (TYLCV) causes huge losses in tomato production worldwide and is caused by different related begomovirus species. Breeding for TYLCV resistance has been based on the introgression of multiple resistance genes originating from several wild tomato species. In this study we have fine-mapped the widely used Solanum chilense-derived Ty-1 and Ty-3 genes by screening nearly 12,000 plants for recombination events and generating recombinant inbred lines. Multiple molecular markers were developed and used in combination with disease tests to fine-map the genes to a small genomic region (approximately 70 kb). Using a Tobacco Rattle Virus-Virus Induced Gene Silencing approach, the resistance gene was identified. It is shown that Ty-1 and Ty-3 are allelic and that they code for a RNA-dependent RNA polymerase (RDR) belonging to the RDRγ type, which has an atypical DFDGD motif in the catalytic domain. In contrast to the RDRα type, characterized by a catalytic DLDGD motif, no clear function has yet been described for the RDRγ type, and thus the Ty-1/Ty-3 gene unveils a completely new class of resistance gene. Although speculative, the resistance mechanism of Ty-1/Ty-3 and its specificity towards TYLCV are discussed in light of the function of the related RDRα class in the amplification of the RNAi response in plants and transcriptional silencing of geminiviruses in plants.
AbstractList Tomato Yellow Leaf Curl Virus Disease incited by Tomato yellow leaf curl virus (TYLCV) causes huge losses in tomato production worldwide and is caused by different related begomovirus species. Breeding for TYLCV resistance has been based on the introgression of multiple resistance genes originating from several wild tomato species. In this study we have fine-mapped the widely used Solanum chilense-derived Ty-1 and Ty-3 genes by screening nearly 12,000 plants for recombination events and generating recombinant inbred lines. Multiple molecular markers were developed and used in combination with disease tests to fine-map the genes to a small genomic region (approximately 70 kb). Using a Tobacco Rattle Virus-Virus Induced Gene Silencing approach, the resistance gene was identified. It is shown that Ty-1 and Ty-3 are allelic and that they code for a RNA-dependent RNA polymerase (RDR) belonging to the RDRy type, which has an atypical DFDGD motif in the catalytic domain. In contrast to the RDRa type, characterized by a catalytic DLDGD motif, no clear function has yet been described for the RDRy type, and thus the Ty-1/Ty-3 gene unveils a completely new class of resistance gene. Although speculative, the resistance mechanism of Ty-1/Ty-3 and its specificity towards TYLCV are discussed in light of the function of the related RDRa class in the amplification of the RNAi response in plants and transcriptional silencing of geminiviruses in plants.
Tomato Yellow Leaf Curl Virus Disease incited by Tomato yellow leaf curl virus (TYLCV) causes huge losses in tomato production worldwide and is caused by different related begomovirus species. Breeding for TYLCV resistance has been based on the introgression of multiple resistance genes originating from several wild tomato species. In this study we have fine-mapped the widely used Solanum chilense-derived Ty-1 and Ty-3 genes by screening nearly 12,000 plants for recombination events and generating recombinant inbred lines. Multiple molecular markers were developed and used in combination with disease tests to fine-map the genes to a small genomic region (approximately 70 kb). Using a Tobacco Rattle Virus-Virus Induced Gene Silencing approach, the resistance gene was identified. It is shown that Ty-1 and Ty-3 are allelic and that they code for a RNA-dependent RNA polymerase (RDR) belonging to the RDRγ type, which has an atypical DFDGD motif in the catalytic domain. In contrast to the RDRα type, characterized by a catalytic DLDGD motif, no clear function has yet been described for the RDRγ type, and thus the Ty-1/Ty-3 gene unveils a completely new class of resistance gene. Although speculative, the resistance mechanism of Ty-1/Ty-3 and its specificity towards TYLCV are discussed in light of the function of the related RDRα class in the amplification of the RNAi response in plants and transcriptional silencing of geminiviruses in plants.Tomato Yellow Leaf Curl Virus Disease incited by Tomato yellow leaf curl virus (TYLCV) causes huge losses in tomato production worldwide and is caused by different related begomovirus species. Breeding for TYLCV resistance has been based on the introgression of multiple resistance genes originating from several wild tomato species. In this study we have fine-mapped the widely used Solanum chilense-derived Ty-1 and Ty-3 genes by screening nearly 12,000 plants for recombination events and generating recombinant inbred lines. Multiple molecular markers were developed and used in combination with disease tests to fine-map the genes to a small genomic region (approximately 70 kb). Using a Tobacco Rattle Virus-Virus Induced Gene Silencing approach, the resistance gene was identified. It is shown that Ty-1 and Ty-3 are allelic and that they code for a RNA-dependent RNA polymerase (RDR) belonging to the RDRγ type, which has an atypical DFDGD motif in the catalytic domain. In contrast to the RDRα type, characterized by a catalytic DLDGD motif, no clear function has yet been described for the RDRγ type, and thus the Ty-1/Ty-3 gene unveils a completely new class of resistance gene. Although speculative, the resistance mechanism of Ty-1/Ty-3 and its specificity towards TYLCV are discussed in light of the function of the related RDRα class in the amplification of the RNAi response in plants and transcriptional silencing of geminiviruses in plants.
  Tomato Yellow Leaf Curl Virus Disease incited by Tomato yellow leaf curl virus (TYLCV) causes huge losses in tomato production worldwide and is caused by different related begomovirus species. Breeding for TYLCV resistance has been based on the introgression of multiple resistance genes originating from several wild tomato species. In this study we have fine-mapped the widely used Solanum chilense-derived Ty-1 and Ty-3 genes by screening nearly 12,000 plants for recombination events and generating recombinant inbred lines. Multiple molecular markers were developed and used in combination with disease tests to fine-map the genes to a small genomic region (approximately 70 kb). Using a Tobacco Rattle Virus-Virus Induced Gene Silencing approach, the resistance gene was identified. It is shown that Ty-1 and Ty-3 are allelic and that they code for a RNA-dependent RNA polymerase (RDR) belonging to the RDRγ type, which has an atypical DFDGD motif in the catalytic domain. In contrast to the RDRα type, characterized by a catalytic DLDGD motif, no clear function has yet been described for the RDRγ type, and thus the Ty-1/Ty-3 gene unveils a completely new class of resistance gene. Although speculative, the resistance mechanism of Ty-1/Ty-3 and its specificity towards TYLCV are discussed in light of the function of the related RDRα class in the amplification of the RNAi response in plants and transcriptional silencing of geminiviruses in plants.
Tomato Yellow Leaf Curl Virus Disease incited by Tomato yellow leaf curl virus (TYLCV) causes huge losses in tomato production worldwide and is caused by different related begomovirus species. Breeding for TYLCV resistance has been based on the introgression of multiple resistance genes originating from several wild tomato species. In this study we have fine-mapped the widely used Solanum chilense-derived Ty-1 and Ty-3 genes by screening nearly 12,000 plants for recombination events and generating recombinant inbred lines. Multiple molecular markers were developed and used in combination with disease tests to fine-map the genes to a small genomic region (approximately 70 kb). Using a Tobacco Rattle Virus-Virus Induced Gene Silencing approach, the resistance gene was identified. It is shown that Ty-1 and Ty-3 are allelic and that they code for a RNA-dependent RNA polymerase (RDR) belonging to the RDRγ type, which has an atypical DFDGD motif in the catalytic domain. In contrast to the RDRα type, characterized by a catalytic DLDGD motif, no clear function has yet been described for the RDRγ type, and thus the Ty-1/Ty-3 gene unveils a completely new class of resistance gene. Although speculative, the resistance mechanism of Ty-1/Ty-3 and its specificity towards TYLCV are discussed in light of the function of the related RDRα class in the amplification of the RNAi response in plants and transcriptional silencing of geminiviruses in plants.
Tomato Yellow Leaf Curl Virus Disease incited by Tomato yellow leaf curl virus (TYLCV) causes huge losses in tomato production worldwide and is caused by different related begomovirus species. Breeding for TYLCV resistance has been based on the introgression of multiple resistance genes originating from several wild tomato species. In this study we have fine-mapped the widely used Solanum chilense–derived Ty-1 and Ty-3 genes by screening nearly 12,000 plants for recombination events and generating recombinant inbred lines. Multiple molecular markers were developed and used in combination with disease tests to fine-map the genes to a small genomic region (approximately 70 kb). Using a Tobacco Rattle Virus–Virus Induced Gene Silencing approach, the resistance gene was identified. It is shown that Ty-1 and Ty-3 are allelic and that they code for a RNA–dependent RNA polymerase (RDR) belonging to the RDR¿ type, which has an atypical DFDGD motif in the catalytic domain. In contrast to the RDRa type, characterized by a catalytic DLDGD motif, no clear function has yet been described for the RDR¿ type, and thus the Ty-1/Ty-3 gene unveils a completely new class of resistance gene. Although speculative, the resistance mechanism of Ty-1/Ty-3 and its specificity towards TYLCV are discussed in light of the function of the related RDRa class in the amplification of the RNAi response in plants and transcriptional silencing of geminiviruses in plants
Tomato Yellow Leaf Curl Virus Disease incited by Tomato yellow leaf curl virus (TYLCV) causes huge losses in tomato production worldwide and is caused by different related begomovirus species. Breeding for TYLCV resistance has been based on the introgression of multiple resistance genes originating from several wild tomato species. In this study we have fine-mapped the widely used Solanum chilense–derived Ty-1 and Ty-3 genes by screening nearly 12,000 plants for recombination events and generating recombinant inbred lines. Multiple molecular markers were developed and used in combination with disease tests to fine-map the genes to a small genomic region (approximately 70 kb). Using a Tobacco Rattle Virus–Virus Induced Gene Silencing approach, the resistance gene was identified. It is shown that Ty-1 and Ty-3 are allelic and that they code for a RNA–dependent RNA polymerase (RDR) belonging to the RDRγ type, which has an atypical DFDGD motif in the catalytic domain. In contrast to the RDRα type, characterized by a catalytic DLDGD motif, no clear function has yet been described for the RDRγ type, and thus the Ty-1/Ty-3 gene unveils a completely new class of resistance gene. Although speculative, the resistance mechanism of Ty-1/Ty-3 and its specificity towards TYLCV are discussed in light of the function of the related RDRα class in the amplification of the RNAi response in plants and transcriptional silencing of geminiviruses in plants. Tomato yellow leaf curl virus and related begomoviruses cause major economic damage to tomato production in tropical and subtropical regions around the world. Because cultivated tomato is inherently susceptible to these viruses, breeders have incorporated several resistance alleles from wild tomato relatives. Among these are the commercially important alleles, Ty-1 and Ty-3, which were introgressed from the wild tomato relative Solanum chilense. These genes were originally mapped to different regions on chromosome 6, but recent findings suggest they may rather be alleles of the same gene. Here, we describe the precise mapping of Ty-1 and Ty-3 to a common chromosomal region, and we show that Ty-1 and Ty-3 are alleles that code for an RNA–dependent RNA polymerase of a class for which no function had been described before. Thus, Ty-1/Ty-3 unveils a completely new class of resistance genes. These results will be useful to breeders who utilize these genes in their breeding programs, and further studies should shed new light on the mechanism by which this gene functions.
Audience Academic
Author Visser, Richard G. F.
Hutton, Samuel F.
Edwards, Jeremy D.
Scott, John W.
Bai, Yuling
Kormelink, Richard
Verlaan, Maarten G.
Ibrahem, Ragy M.
AuthorAffiliation 2 Centre for BioSystems Genomics, Wageningen, The Netherlands
5 Laboratory of Virology, Wageningen University and Research Centre, Wageningen, The Netherlands
4 Gulf Coast Research and Education Center, University of Florida, Wimauma, Florida, United States of America
Virginia Tech, United States of America
3 Graduate School Experimental Plant Sciences, Wageningen University and Research Centre, Wageningen, The Netherlands
1 Wageningen UR Plant Breeding, Wageningen University and Research Centre, Wageningen, The Netherlands
AuthorAffiliation_xml – name: Virginia Tech, United States of America
– name: 4 Gulf Coast Research and Education Center, University of Florida, Wimauma, Florida, United States of America
– name: 1 Wageningen UR Plant Breeding, Wageningen University and Research Centre, Wageningen, The Netherlands
– name: 2 Centre for BioSystems Genomics, Wageningen, The Netherlands
– name: 5 Laboratory of Virology, Wageningen University and Research Centre, Wageningen, The Netherlands
– name: 3 Graduate School Experimental Plant Sciences, Wageningen University and Research Centre, Wageningen, The Netherlands
Author_xml – sequence: 1
  givenname: Maarten G.
  surname: Verlaan
  fullname: Verlaan, Maarten G.
– sequence: 2
  givenname: Samuel F.
  surname: Hutton
  fullname: Hutton, Samuel F.
– sequence: 3
  givenname: Ragy M.
  surname: Ibrahem
  fullname: Ibrahem, Ragy M.
– sequence: 4
  givenname: Richard
  surname: Kormelink
  fullname: Kormelink, Richard
– sequence: 5
  givenname: Richard G. F.
  surname: Visser
  fullname: Visser, Richard G. F.
– sequence: 6
  givenname: John W.
  surname: Scott
  fullname: Scott, John W.
– sequence: 7
  givenname: Jeremy D.
  surname: Edwards
  fullname: Edwards, Jeremy D.
– sequence: 8
  givenname: Yuling
  surname: Bai
  fullname: Bai, Yuling
BackLink https://www.ncbi.nlm.nih.gov/pubmed/23555305$$D View this record in MEDLINE/PubMed
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2013 Verlaan et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Verlaan MG, Hutton SF, Ibrahem RM, Kormelink R, Visser RGF, et al. (2013) The Tomato Yellow Leaf Curl Virus Resistance Genes Ty-1 and Ty-3 Are Allelic and Code for DFDGD-Class RNA-Dependent RNA Polymerases. PLoS Genet 9(3): e1003399. doi:10.1371/journal.pgen.1003399
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– notice: 2013 Verlaan et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Verlaan MG, Hutton SF, Ibrahem RM, Kormelink R, Visser RGF, et al. (2013) The Tomato Yellow Leaf Curl Virus Resistance Genes Ty-1 and Ty-3 Are Allelic and Code for DFDGD-Class RNA-Dependent RNA Polymerases. PLoS Genet 9(3): e1003399. doi:10.1371/journal.pgen.1003399
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Conceived and designed the experiments: MGV SFH RK JWS JDE YB. Performed the experiments: MGV SFH RMI. Analyzed the data: MGV SFH RK JWS YB. Contributed reagents/materials/analysis tools: MGV SFH RK JWS RGFV YB. Wrote the paper: MGV SFH RK RGFV JWS YB.
The authors have declared that no competing interests exist.
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Snippet Tomato Yellow Leaf Curl Virus Disease incited by Tomato yellow leaf curl virus (TYLCV) causes huge losses in tomato production worldwide and is caused by...
  Tomato Yellow Leaf Curl Virus Disease incited by Tomato yellow leaf curl virus (TYLCV) causes huge losses in tomato production worldwide and is caused by...
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SubjectTerms adenosine kinase
Agriculture
Alleles
Begomovirus - genetics
Begomovirus - pathogenicity
Biology
breeding lines
Chromosomes
Disease Resistance - genetics
Diseases and pests
geminivirus al2
Genes
Genetic aspects
Genetics
Genomes
Genomics
Health aspects
Host-parasite relationships
interfering rnas
l2 proteins
lycopersicon-chilense
mottle virus
nicotiana-attenuata
Physiological aspects
Plant Diseases - genetics
Plant Diseases - virology
Plant immunology
Plant Leaves - genetics
Plant Leaves - virology
Plant viruses
recessive resistance
RNA - genetics
RNA Interference
RNA polymerase
RNA polymerases
RNA-Dependent RNA Polymerase - genetics
RNA-Dependent RNA Polymerase - metabolism
Solanum lycopersicum - genetics
Solanum lycopersicum - virology
Tomatoes
Viral genetics
Virus diseases of plants
Viruses
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Title The Tomato Yellow Leaf Curl Virus Resistance Genes Ty-1 and Ty-3 Are Allelic and Code for DFDGD-Class RNA–Dependent RNA Polymerases
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