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Article: Wheat powdery mildew resistance: from gene identification to immunity deployment.

Zou, Shenghao / Xu, Yang / Li, Qianqian / Wei, Yali / Zhang, Youlian / Tang, Dingzhong

2023 Volume 14, Page(s) 1269498

Abstract: Powdery mildew is one of the most devastating diseases on wheat and is caused by the obligate biotrophic ... ...

Abstract	Powdery mildew is one of the most devastating diseases on wheat and is caused by the obligate biotrophic phytopathogen
Language	English
Publishing date	2023-09-18
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2613694-6
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2023.1269498
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Article: Diversity and similarity of wheat powdery mildew resistance among three allelic functional genes at the Pm60 locus

Zou, Shenghao / Shi, Wenqi / Ji, Jiahao / Wang, Huanming / Tang, Yansheng / Yu, Dazhao / Tang, Dingzhong

plant journal. 2022 June, v. 110, no. 6

2022

Abstract: Cultivated wheat is continually exposed to various pathogens. Blumeria graminis f. sp. tritici (Bgt) causes powdery mildew disease and significant yield loss. Pm60 was cloned from Triticum urartu and confers race‐specific powdery mildew resistance in ... ...

Abstract	Cultivated wheat is continually exposed to various pathogens. Blumeria graminis f. sp. tritici (Bgt) causes powdery mildew disease and significant yield loss. Pm60 was cloned from Triticum urartu and confers race‐specific powdery mildew resistance in wheat. Pm60a and Pm60b are allelic variants of Pm60 and have two leucine‐rich repeat motifs deletions and insertions, respectively, which were detected in other T. urartu accessions. Through map‐based cloning, virus‐induced gene silencing, and stable transformation assays, we demonstrated that Pm60a and Pm60b conferred Bgt E09 resistance resembling that provided by Pm60. However, the homozygous Pm60a (but not Pm60 or Pm60b) transformants driven by the native promoters lacked race‐specific resistance when they were inoculated with Bgt E18. As all three T. urartu accessions contained the three foregoing alleles, they had high resistance to Bgt E18. Pyramiding Pm60a with either of the allelic genes in F₁ plants did not cause mutual allele suppression or interference with Bgt E18 resistance. Deletion (but not insertion) of the two leucine‐rich repeat motifs in Pm60a substantially narrowed the resistance spectrum. In T. urartu accession PI428210, we identified another locus adjacent to Pm60a and resistant to Bgt E18. Characterization of the alleles at the Pm60 locus revealed their diversity and similarity and may facilitate wheat breeding for resistance to powdery mildew disease caused by B. graminis f. sp. tritici.
Keywords	Triticum urartu ; alleles ; homozygosity ; loci ; powdery mildew ; wheat
Language	English
Dates of publication	2022-06
Size	p. 1781-1790.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/tpj.15771
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Article ; Online: A NAC Transcription Factor TuNAC69 Contributes to ANK-NLR-WRKY NLR-Mediated Stripe Rust Resistance in the Diploid Wheat

Xu, Yang / Zou, Shenghao / Zeng, Hao / Wang, Wei / Wang, Bin / Wang, Huan / Tang, Dingzhong

International journal of molecular sciences

2022 Volume 23, Issue 1

Abstract: Stripe rust is one of the most devastating diseases in wheat. Nucleotide-binding site (NBS) and leucine-rich repeat (LRR) domain receptors (NLRs) recognize pathogenic effectors and trigger plant immunity. We previously identified a unique NLR protein ... ...

Abstract	Stripe rust is one of the most devastating diseases in wheat. Nucleotide-binding site (NBS) and leucine-rich repeat (LRR) domain receptors (NLRs) recognize pathogenic effectors and trigger plant immunity. We previously identified a unique NLR protein YrU1 in the diploid wheat
MeSH term(s)	Amino Acid Sequence ; Ankyrin Repeat ; Conserved Sequence ; Diploidy ; Disease Resistance/genetics ; Evolution, Molecular ; Gene Expression Regulation, Plant ; Gene Knockdown Techniques ; Host-Pathogen Interactions/genetics ; Multigene Family ; NLR Proteins ; Phenotype ; Phylogeny ; Plant Diseases/genetics ; Plant Diseases/microbiology ; Plant Proteins/genetics ; Plant Proteins/metabolism ; Trans-Activators/chemistry ; Trans-Activators/genetics ; Trans-Activators/metabolism ; Triticum/classification ; Triticum/genetics ; Triticum/metabolism ; Triticum/microbiology
Chemical Substances	NLR Proteins ; Plant Proteins ; Trans-Activators
Language	English
Publishing date	2022-01-05
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms23010564
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Article ; Online: Diversity and similarity of wheat powdery mildew resistance among three allelic functional genes at the Pm60 locus.

Zou, Shenghao / Shi, Wenqi / Ji, Jiahao / Wang, Huanming / Tang, Yansheng / Yu, Dazhao / Tang, Dingzhong

The Plant journal : for cell and molecular biology

2022 Volume 110, Issue 6, Page(s) 1781–1790

Abstract	Cultivated wheat is continually exposed to various pathogens. Blumeria graminis f. sp. tritici (Bgt) causes powdery mildew disease and significant yield loss. Pm60 was cloned from Triticum urartu and confers race-specific powdery mildew resistance in wheat. Pm60a and Pm60b are allelic variants of Pm60 and have two leucine-rich repeat motifs deletions and insertions, respectively, which were detected in other T. urartu accessions. Through map-based cloning, virus-induced gene silencing, and stable transformation assays, we demonstrated that Pm60a and Pm60b conferred Bgt E09 resistance resembling that provided by Pm60. However, the homozygous Pm60a (but not Pm60 or Pm60b) transformants driven by the native promoters lacked race-specific resistance when they were inoculated with Bgt E18. As all three T. urartu accessions contained the three foregoing alleles, they had high resistance to Bgt E18. Pyramiding Pm60a with either of the allelic genes in F
MeSH term(s)	Alleles ; Ascomycota ; Disease Resistance/genetics ; Leucine ; Plant Breeding ; Plant Diseases/genetics ; Triticum/genetics
Chemical Substances	Leucine (GMW67QNF9C)
Language	English
Publishing date	2022-04-29
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/tpj.15771
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: TuRLK1, a leucine-rich repeat receptor-like kinase, is indispensable for stripe rust resistance of YrU1 and confers broad resistance to multiple pathogens

Zou, Shenghao / Tang, Yansheng / Xu, Yang / Ji, Jiahao / Lu, Yuanyuan / Wang, Huanming / Li, Qianqian / Tang, Dingzhong

BMC Plant Biol. 2022 Dec., v. 22, no. 1 p.280-280

2022

Abstract: BACKGROUND: YrU1 is a nucleotide-binding site (NBS) and leucine-rich repeat (LRR) protein (NLR), with additional ankyrin-repeat and WRKY domains and confers effective resistance to stripe rust fungus Puccinia striiformis f. sp. Tritici (Pst). YrU1 was ... ...

Abstract	BACKGROUND: YrU1 is a nucleotide-binding site (NBS) and leucine-rich repeat (LRR) protein (NLR), with additional ankyrin-repeat and WRKY domains and confers effective resistance to stripe rust fungus Puccinia striiformis f. sp. Tritici (Pst). YrU1 was positionally cloned in the progenitor species of the A genome of bread wheat, Tricicum urartu, recently. However, the molecular mechanism and components involved in YrU1-mediated resistance are not clear. RESULTS: In this study, we found that the transcript level of TuRLK1, which encodes a novel leucine-rich repeat receptor-like kinase, was up-regulated after inoculation with Pst in the presence of YrU1, through RNA-seq analysis in T. urartu accession PI428309. TuRLK1 contained only a small number of LRR motifs, and was localized in the plasma-membrane. Transient expression of TuRLK1 induced hypersensitive cell death response in N. benthamiana leaves. Silencing of TuRLK1, using barley stripe mosaic virus (BSMV)-induced gene silencing (VIGS) system in PI428309 that contains YrU1, compromised the resistance against stripe rust caused by Pst CY33, indicating that TuRLK1 was required for YrU1-activated plant immunity. Furthermore, overexpression of TuRLK1 could enhance powdery mildew resistance in bread wheat and Arabidopsis thaliana after inoculating with the corresponding pathogens. CONCLUSIONS: Our study indicates that TuRLK1 is required for immune response mediated by the unique NLR protein YrU1, and likely plays an important role in disease resistance to other pathogens.
Keywords	Arabidopsis thaliana ; Barley stripe mosaic virus ; Puccinia striiformis f. tritici ; cell death ; disease resistance ; fungi ; genes ; immune response ; plasma membrane ; powdery mildew ; sequence analysis ; stripe rust ; wheat
Language	English
Dates of publication	2022-12
Size	p. 280.
Publishing place	BioMed Central
Document type	Article ; Online
ZDB-ID	2059868-3
ISSN	1471-2229
ISSN	1471-2229
DOI	10.1186/s12870-022-03679-6
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Article ; Online: An ankyrin-repeat and WRKY-domain-containing immune receptor confers stripe rust resistance in wheat.

Wang, Huan / Zou, Shenghao / Li, Yiwen / Lin, Fanyun / Tang, Dingzhong

Nature communications

2020 Volume 11, Issue 1, Page(s) 1353

Abstract: Perception of pathogenic effectors in plants often relies on nucleotide-binding domain (NBS) and leucine-rich-repeat-containing (NLR) proteins. Some NLRs contain additional domains that function as integrated decoys for pathogen effector targets and ... ...

Abstract	Perception of pathogenic effectors in plants often relies on nucleotide-binding domain (NBS) and leucine-rich-repeat-containing (NLR) proteins. Some NLRs contain additional domains that function as integrated decoys for pathogen effector targets and activation of immune signalling. Wheat stripe rust is one of the most devastating diseases of crop plants. Here, we report the cloning of YrU1, a stripe rust resistance gene from the diploid wheat Triticum urartu, the progenitor of the A genome of hexaploid wheat. YrU1 encodes a coiled-coil-NBS-leucine-rich repeat protein with N-terminal ankyrin-repeat and C-terminal WRKY domains, representing a unique NLR structure in plants. Database searches identify similar architecture only in wheat relatives. Transient expression of YrU1 in Nicotiana benthamiana does not induce cell death in the absence of pathogens. The ankyrin-repeat and coiled-coil domains of YrU1 self-associate, suggesting that homodimerisation is critical for YrU1 function. The identification and cloning of this disease resistance gene sheds light on NLR protein function and may facilitate breeding to control the devastating wheat stripe rust disease.
MeSH term(s)	Ankyrin Repeat/genetics ; Ankyrin Repeat/physiology ; Ankyrins/genetics ; Ankyrins/metabolism ; Basidiomycota ; Cloning, Molecular ; DNA-Binding Proteins/genetics ; DNA-Binding Proteins/metabolism ; Disease Resistance/genetics ; Disease Resistance/physiology ; Gene Expression Regulation, Plant ; Gene Knockdown Techniques ; Genes, Plant ; NLR Proteins ; Plant Diseases/immunology ; Plant Diseases/microbiology ; Plant Immunity/genetics ; Plant Immunity/physiology ; Plant Proteins/genetics ; Plants, Genetically Modified/metabolism ; Nicotiana/genetics ; Nicotiana/metabolism ; Transcription Factors/genetics ; Transcription Factors/metabolism ; Transcriptome ; Triticum/genetics ; Triticum/immunology
Chemical Substances	Ankyrins ; DNA-Binding Proteins ; NLR Proteins ; Plant Proteins ; Transcription Factors
Language	English
Publishing date	2020-03-13
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-020-15139-6
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Article ; Online: TuRLK1, a leucine-rich repeat receptor-like kinase, is indispensable for stripe rust resistance of YrU1 and confers broad resistance to multiple pathogens.

Zou, Shenghao / Tang, Yansheng / Xu, Yang / Ji, Jiahao / Lu, Yuanyuan / Wang, Huanming / Li, Qianqian / Tang, Dingzhong

BMC plant biology

2022 Volume 22, Issue 1, Page(s) 280

Abstract: Background: YrU1 is a nucleotide-binding site (NBS) and leucine-rich repeat (LRR) protein (NLR), with additional ankyrin-repeat and WRKY domains and confers effective resistance to stripe rust fungus Puccinia striiformis f. sp. Tritici (Pst). YrU1 was ... ...

Abstract	Background: YrU1 is a nucleotide-binding site (NBS) and leucine-rich repeat (LRR) protein (NLR), with additional ankyrin-repeat and WRKY domains and confers effective resistance to stripe rust fungus Puccinia striiformis f. sp. Tritici (Pst). YrU1 was positionally cloned in the progenitor species of the A genome of bread wheat, Tricicum urartu, recently. However, the molecular mechanism and components involved in YrU1-mediated resistance are not clear. Results: In this study, we found that the transcript level of TuRLK1, which encodes a novel leucine-rich repeat receptor-like kinase, was up-regulated after inoculation with Pst in the presence of YrU1, through RNA-seq analysis in T. urartu accession PI428309. TuRLK1 contained only a small number of LRR motifs, and was localized in the plasma-membrane. Transient expression of TuRLK1 induced hypersensitive cell death response in N. benthamiana leaves. Silencing of TuRLK1, using barley stripe mosaic virus (BSMV)-induced gene silencing (VIGS) system in PI428309 that contains YrU1, compromised the resistance against stripe rust caused by Pst CY33, indicating that TuRLK1 was required for YrU1-activated plant immunity. Furthermore, overexpression of TuRLK1 could enhance powdery mildew resistance in bread wheat and Arabidopsis thaliana after inoculating with the corresponding pathogens. Conclusions: Our study indicates that TuRLK1 is required for immune response mediated by the unique NLR protein YrU1, and likely plays an important role in disease resistance to other pathogens.
MeSH term(s)	Arabidopsis ; Basidiomycota/physiology ; Disease Resistance/genetics ; Leucine/metabolism ; Plant Diseases/microbiology ; Triticum/metabolism
Chemical Substances	Leucine (GMW67QNF9C)
Language	English
Publishing date	2022-06-08
Publishing country	England
Document type	Journal Article
ZDB-ID	2059868-3
ISSN	1471-2229 ; 1471-2229
ISSN (online)	1471-2229
ISSN	1471-2229
DOI	10.1186/s12870-022-03679-6
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Article ; Online: The NB-LRR gene Pm60 confers powdery mildew resistance in wheat.

Zou, Shenghao / Wang, Huan / Li, Yiwen / Kong, Zhaosheng / Tang, Dingzhong

The New phytologist

2017 Volume 218, Issue 1, Page(s) 298–309

Abstract: Powdery mildew is one of the most devastating diseases of wheat. To date, few powdery mildew resistance genes have been cloned from wheat due to the size and complexity of the wheat genome. Triticum urartu is the progenitor of the A genome of wheat and ... ...

Abstract	Powdery mildew is one of the most devastating diseases of wheat. To date, few powdery mildew resistance genes have been cloned from wheat due to the size and complexity of the wheat genome. Triticum urartu is the progenitor of the A genome of wheat and is an important source for powdery mildew resistance genes. Using molecular markers designed from scaffolds of the sequenced T. urartu accession and standard map-based cloning, a powdery mildew resistance locus was mapped to a 356-kb region, which contains two nucleotide-binding and leucine-rich repeat domain (NB-LRR) protein-encoding genes. Virus-induced gene silencing, single-cell transient expression, and stable transformation assays demonstrated that one of these two genes, designated Pm60, confers resistance to powdery mildew. Overexpression of full-length Pm60 and two allelic variants in Nicotiana benthamiana leaves induced hypersensitive cell death response, but expression of the coiled-coil domain alone was insufficient to induce hypersensitive response. Yeast two-hybrid, bimolecular fluorescence complementation and luciferase complementation imaging assays showed that Pm60 protein interacts with its neighboring NB-containing protein, suggesting that they might be functionally related. The identification and cloning of this novel wheat powdery mildew resistance gene will facilitate breeding for disease resistance in wheat.
MeSH term(s)	Alleles ; Ascomycota/physiology ; Base Sequence ; Cell Death ; Disease Resistance/genetics ; Gene Silencing ; Genes, Plant ; Genetic Loci ; Physical Chromosome Mapping ; Plant Diseases/genetics ; Plant Diseases/immunology ; Plant Diseases/microbiology ; Plant Leaves/cytology ; Plant Proteins/chemistry ; Plant Proteins/genetics ; Plant Proteins/metabolism ; Plants, Genetically Modified ; Protein Domains ; Single-Cell Analysis ; Nicotiana/genetics ; Transformation, Genetic ; Triticum/genetics ; Triticum/immunology ; Triticum/microbiology
Chemical Substances	Plant Proteins
Language	English
Publishing date	2017-12-27
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.14964
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: The NB‐LRR gene Pm60 confers powdery mildew resistance in wheat

Zou, Shenghao / Huan Wang / Yiwen Li / Zhaosheng Kong / Dingzhong Tang

new phytologist. 2018 Apr., v. 218, no. 1

2018

Abstract	Powdery mildew is one of the most devastating diseases of wheat. To date, few powdery mildew resistance genes have been cloned from wheat due to the size and complexity of the wheat genome. Triticum urartu is the progenitor of the A genome of wheat and is an important source for powdery mildew resistance genes. Using molecular markers designed from scaffolds of the sequenced T. urartu accession and standard map‐based cloning, a powdery mildew resistance locus was mapped to a 356‐kb region, which contains two nucleotide‐binding and leucine‐rich repeat domain (NB‐LRR) protein‐encoding genes. Virus‐induced gene silencing, single‐cell transient expression, and stable transformation assays demonstrated that one of these two genes, designated Pm60, confers resistance to powdery mildew. Overexpression of full‐length Pm60 and two allelic variants in Nicotiana benthamiana leaves induced hypersensitive cell death response, but expression of the coiled‐coil domain alone was insufficient to induce hypersensitive response. Yeast two‐hybrid, bimolecular fluorescence complementation and luciferase complementation imaging assays showed that Pm60 protein interacts with its neighboring NB‐containing protein, suggesting that they might be functionally related. The identification and cloning of this novel wheat powdery mildew resistance gene will facilitate breeding for disease resistance in wheat.
Keywords	Nicotiana benthamiana ; Triticum urartu ; breeding ; cell death ; disease resistance ; fluorescence ; gene overexpression ; gene silencing ; genetic markers ; hypersensitive response ; image analysis ; leaves ; loci ; luciferase ; powdery mildew ; resistance genes ; two hybrid system techniques ; wheat
Language	English
Dates of publication	2018-04
Size	p. 298-309.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.14964
Database	NAL-Catalogue (AGRICOLA)

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Article: Utility of Triti-Map for bulk-segregated mapping of causal genes and regulatory elements in Triticeae

Zhao, Fei / Tian, Shilong / Wu, Qiuhong / Li, Zijuan / Ye, Luhuan / Zhuang, Yili / Wang, Meiyue / Xie, Yilin / Zou, Shenghao / Teng, Wan / Tong, Yiping / Tang, Dingzhong / Mahato, Ajay Kumar / Benhamed, Moussa / Liu, Zhiyong / Zhang, Yijing

Plant communications. 2022 Feb. 13,

2022

Abstract: Triticeae species, including wheat, barley, and rye, are critical for global food security. Mapping agronomically important genes is crucial for elucidating molecular mechanisms and improving crops. However, Triticeae includes many wild relatives with ... ...

Abstract	Triticeae species, including wheat, barley, and rye, are critical for global food security. Mapping agronomically important genes is crucial for elucidating molecular mechanisms and improving crops. However, Triticeae includes many wild relatives with desirable agronomic traits, and frequent introgressions occurred during Triticeae evolution and domestication. Thus, Triticeae genomes are generally large and complex, making the localization of genes or functional elements that control agronomic traits challenging. Here, we developed Triti-Map, which contains a suite of user-friendly computational packages specifically designed and optimized to overcome the obstacles of gene mapping in Triticeae, as well as a web interface integrating multi-omics data from Triticeae for the efficient mining of genes or functional elements that control particular traits. The Triti-Map pipeline accepts both DNA and RNA bulk-segregated sequencing data as well as traditional QTL data as inputs for locating genes and elucidating their functions. We illustrate the usage of Triti-Map with a combination of bulk-segregated ChIP-seq data to detect a wheat disease-resistance gene with its promoter sequence that is absent from the reference genome and clarify its evolutionary process. We hope that Triti-Map will facilitate gene isolation and accelerate Triticeae breeding.
Keywords	DNA ; RNA ; barley ; chromatin immunoprecipitation ; disease resistance ; domestication ; evolution ; food security ; genes ; multiomics ; promoter regions ; rye ; user interface ; wheat
Language	English
Dates of publication	2022-0213
Publishing place	Elsevier Inc.
Document type	Article
Note	Pre-press version
ISSN	2590-3462
DOI	10.1016/j.xplc.2022.100304
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