An Avirulence Gene Cluster in the Wheat Stripe Rust Pathogen (<named-content content-type="genus-species">Puccinia striiformis</named-content> f. sp. <italic toggle="yes">tritici</italic>) Identified through Genetic Mapping and Whole-Genome Sequencing of a Sexual Population

ABSTRACT Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe (yellow) rust, is an obligate, biotrophic fungus. It was difficult to study the genetics of the pathogen due to the lack of sexual reproduction. The recent discovery of alternate hosts for P. striiformis f. sp. tritici ma...

Full description

Bibliographic Details
Main Authors: Chongjing Xia, Yu Lei, Meinan Wang, Wanquan Chen, Xianming Chen
Format: Article
Language:English
Published: American Society for Microbiology 2020-06-01
Series:mSphere
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mSphere.00128-20
_version_ 1818936015186821120
author Chongjing Xia
Yu Lei
Meinan Wang
Wanquan Chen
Xianming Chen
author_facet Chongjing Xia
Yu Lei
Meinan Wang
Wanquan Chen
Xianming Chen
author_sort Chongjing Xia
collection DOAJ
description ABSTRACT Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe (yellow) rust, is an obligate, biotrophic fungus. It was difficult to study the genetics of the pathogen due to the lack of sexual reproduction. The recent discovery of alternate hosts for P. striiformis f. sp. tritici makes it possible to study inheritance and map genes involved in its interaction with plant hosts. To identify avirulence (Avr) genes in P. striiformis f. sp. tritici, we developed a segregating population by selfing isolate 12-368 on barberry (Berberis vulgaris) plants under controlled conditions. The dikaryotic sexual population segregated for avirulent/virulent phenotypes on nine Yr single-gene lines. The parental and progeny isolates were whole-genome sequenced at >30× coverage using Illumina HiSeq PE150 technology. A total of 2,637 high-quality markers were discovered by mapping the whole-genome sequencing (WGS) reads to the reference genome of strain 93-210 and used to construct a genetic map, consisting of 41 linkage groups, spanning 7,715.0 centimorgans (cM) and covering 68 Mb of the reference genome. The recombination rate was estimated to be 1.81 ± 2.32 cM/10 kb. Quantitative trait locus analysis mapped six Avr gene loci to the genetic map, including an Avr cluster harboring four Avr genes, AvYr7, AvYr43, AvYr44, and AvYrExp2. Aligning the genetic map to the reference genome identified Avr candidates and narrowed them to a small genomic region (<200 kb). The discovery of the Avr gene cluster is useful for understanding pathogen evolution, and the identification of candidate genes is an important step toward cloning Avr genes for studying molecular mechanisms of pathogen-host interactions. IMPORTANCE Stripe rust is a destructive disease of wheat worldwide. Growing resistant cultivars is the most effective, easy-to-use, economical, and environmentally friendly strategy for the control of the disease. However, P. striiformis f. sp. tritici can produce new virulent races that may circumvent race-specific resistance. Therefore, understanding the genetic basis of the interactions between wheat genes for resistance and P. striiformis f. sp. tritici genes for avirulence is useful for improving cultivar resistance for more effective control of the disease. This study developed a high-quality map that facilitates genomic and genetic studies of important traits related to pathogen pathogenicity and adaptation to different environments and crop cultivars carrying different resistance genes. The information on avirulence/virulence genes identified in this study can be used for guiding breeding programs to select combinations of genes for developing new cultivars with effective resistance to mitigate this devastating disease.
first_indexed 2024-12-20T05:29:20Z
format Article
id doaj.art-1b9adc6a1b534176ac0225b1d85a7538
institution Directory Open Access Journal
issn 2379-5042
language English
last_indexed 2024-12-20T05:29:20Z
publishDate 2020-06-01
publisher American Society for Microbiology
record_format Article
series mSphere
spelling doaj.art-1b9adc6a1b534176ac0225b1d85a75382022-12-21T19:51:48ZengAmerican Society for MicrobiologymSphere2379-50422020-06-015310.1128/mSphere.00128-20An Avirulence Gene Cluster in the Wheat Stripe Rust Pathogen (<named-content content-type="genus-species">Puccinia striiformis</named-content> f. sp. <italic toggle="yes">tritici</italic>) Identified through Genetic Mapping and Whole-Genome Sequencing of a Sexual PopulationChongjing Xia0Yu Lei1Meinan Wang2Wanquan Chen3Xianming Chen4Wheat Research Institute, School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, Sichuan, ChinaDepartment of Plant Pathology, Washington State University, Pullman, Washington, USADepartment of Plant Pathology, Washington State University, Pullman, Washington, USAState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, ChinaDepartment of Plant Pathology, Washington State University, Pullman, Washington, USAABSTRACT Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe (yellow) rust, is an obligate, biotrophic fungus. It was difficult to study the genetics of the pathogen due to the lack of sexual reproduction. The recent discovery of alternate hosts for P. striiformis f. sp. tritici makes it possible to study inheritance and map genes involved in its interaction with plant hosts. To identify avirulence (Avr) genes in P. striiformis f. sp. tritici, we developed a segregating population by selfing isolate 12-368 on barberry (Berberis vulgaris) plants under controlled conditions. The dikaryotic sexual population segregated for avirulent/virulent phenotypes on nine Yr single-gene lines. The parental and progeny isolates were whole-genome sequenced at >30× coverage using Illumina HiSeq PE150 technology. A total of 2,637 high-quality markers were discovered by mapping the whole-genome sequencing (WGS) reads to the reference genome of strain 93-210 and used to construct a genetic map, consisting of 41 linkage groups, spanning 7,715.0 centimorgans (cM) and covering 68 Mb of the reference genome. The recombination rate was estimated to be 1.81 ± 2.32 cM/10 kb. Quantitative trait locus analysis mapped six Avr gene loci to the genetic map, including an Avr cluster harboring four Avr genes, AvYr7, AvYr43, AvYr44, and AvYrExp2. Aligning the genetic map to the reference genome identified Avr candidates and narrowed them to a small genomic region (<200 kb). The discovery of the Avr gene cluster is useful for understanding pathogen evolution, and the identification of candidate genes is an important step toward cloning Avr genes for studying molecular mechanisms of pathogen-host interactions. IMPORTANCE Stripe rust is a destructive disease of wheat worldwide. Growing resistant cultivars is the most effective, easy-to-use, economical, and environmentally friendly strategy for the control of the disease. However, P. striiformis f. sp. tritici can produce new virulent races that may circumvent race-specific resistance. Therefore, understanding the genetic basis of the interactions between wheat genes for resistance and P. striiformis f. sp. tritici genes for avirulence is useful for improving cultivar resistance for more effective control of the disease. This study developed a high-quality map that facilitates genomic and genetic studies of important traits related to pathogen pathogenicity and adaptation to different environments and crop cultivars carrying different resistance genes. The information on avirulence/virulence genes identified in this study can be used for guiding breeding programs to select combinations of genes for developing new cultivars with effective resistance to mitigate this devastating disease.https://journals.asm.org/doi/10.1128/mSphere.00128-20avirulencegeneticshost-pathogen interactionPuccinia striiformisQTL mappingwheat stripe rust
spellingShingle Chongjing Xia
Yu Lei
Meinan Wang
Wanquan Chen
Xianming Chen
An Avirulence Gene Cluster in the Wheat Stripe Rust Pathogen (<named-content content-type="genus-species">Puccinia striiformis</named-content> f. sp. <italic toggle="yes">tritici</italic>) Identified through Genetic Mapping and Whole-Genome Sequencing of a Sexual Population
mSphere
avirulence
genetics
host-pathogen interaction
Puccinia striiformis
QTL mapping
wheat stripe rust
title An Avirulence Gene Cluster in the Wheat Stripe Rust Pathogen (<named-content content-type="genus-species">Puccinia striiformis</named-content> f. sp. <italic toggle="yes">tritici</italic>) Identified through Genetic Mapping and Whole-Genome Sequencing of a Sexual Population
title_full An Avirulence Gene Cluster in the Wheat Stripe Rust Pathogen (<named-content content-type="genus-species">Puccinia striiformis</named-content> f. sp. <italic toggle="yes">tritici</italic>) Identified through Genetic Mapping and Whole-Genome Sequencing of a Sexual Population
title_fullStr An Avirulence Gene Cluster in the Wheat Stripe Rust Pathogen (<named-content content-type="genus-species">Puccinia striiformis</named-content> f. sp. <italic toggle="yes">tritici</italic>) Identified through Genetic Mapping and Whole-Genome Sequencing of a Sexual Population
title_full_unstemmed An Avirulence Gene Cluster in the Wheat Stripe Rust Pathogen (<named-content content-type="genus-species">Puccinia striiformis</named-content> f. sp. <italic toggle="yes">tritici</italic>) Identified through Genetic Mapping and Whole-Genome Sequencing of a Sexual Population
title_short An Avirulence Gene Cluster in the Wheat Stripe Rust Pathogen (<named-content content-type="genus-species">Puccinia striiformis</named-content> f. sp. <italic toggle="yes">tritici</italic>) Identified through Genetic Mapping and Whole-Genome Sequencing of a Sexual Population
title_sort avirulence gene cluster in the wheat stripe rust pathogen named content content type genus species puccinia striiformis named content f sp italic toggle yes tritici italic identified through genetic mapping and whole genome sequencing of a sexual population
topic avirulence
genetics
host-pathogen interaction
Puccinia striiformis
QTL mapping
wheat stripe rust
url https://journals.asm.org/doi/10.1128/mSphere.00128-20
work_keys_str_mv AT chongjingxia anavirulencegeneclusterinthewheatstriperustpathogennamedcontentcontenttypegenusspeciespucciniastriiformisnamedcontentfspitalictoggleyestriticiitalicidentifiedthroughgeneticmappingandwholegenomesequencingofasexualpopulation
AT yulei anavirulencegeneclusterinthewheatstriperustpathogennamedcontentcontenttypegenusspeciespucciniastriiformisnamedcontentfspitalictoggleyestriticiitalicidentifiedthroughgeneticmappingandwholegenomesequencingofasexualpopulation
AT meinanwang anavirulencegeneclusterinthewheatstriperustpathogennamedcontentcontenttypegenusspeciespucciniastriiformisnamedcontentfspitalictoggleyestriticiitalicidentifiedthroughgeneticmappingandwholegenomesequencingofasexualpopulation
AT wanquanchen anavirulencegeneclusterinthewheatstriperustpathogennamedcontentcontenttypegenusspeciespucciniastriiformisnamedcontentfspitalictoggleyestriticiitalicidentifiedthroughgeneticmappingandwholegenomesequencingofasexualpopulation
AT xianmingchen anavirulencegeneclusterinthewheatstriperustpathogennamedcontentcontenttypegenusspeciespucciniastriiformisnamedcontentfspitalictoggleyestriticiitalicidentifiedthroughgeneticmappingandwholegenomesequencingofasexualpopulation
AT chongjingxia avirulencegeneclusterinthewheatstriperustpathogennamedcontentcontenttypegenusspeciespucciniastriiformisnamedcontentfspitalictoggleyestriticiitalicidentifiedthroughgeneticmappingandwholegenomesequencingofasexualpopulation
AT yulei avirulencegeneclusterinthewheatstriperustpathogennamedcontentcontenttypegenusspeciespucciniastriiformisnamedcontentfspitalictoggleyestriticiitalicidentifiedthroughgeneticmappingandwholegenomesequencingofasexualpopulation
AT meinanwang avirulencegeneclusterinthewheatstriperustpathogennamedcontentcontenttypegenusspeciespucciniastriiformisnamedcontentfspitalictoggleyestriticiitalicidentifiedthroughgeneticmappingandwholegenomesequencingofasexualpopulation
AT wanquanchen avirulencegeneclusterinthewheatstriperustpathogennamedcontentcontenttypegenusspeciespucciniastriiformisnamedcontentfspitalictoggleyestriticiitalicidentifiedthroughgeneticmappingandwholegenomesequencingofasexualpopulation
AT xianmingchen avirulencegeneclusterinthewheatstriperustpathogennamedcontentcontenttypegenusspeciespucciniastriiformisnamedcontentfspitalictoggleyestriticiitalicidentifiedthroughgeneticmappingandwholegenomesequencingofasexualpopulation