Genetic analysis of wheat sensitivity to the ToxB fungal effector from Pyrenophora tritici-repentis, the causal agent of tan spot

Corsi, Beatrice; Percival‐Alwyn, Lawrence; Downie, Rowena; Venturini, Luca; Iagallo, E.; Mantello, Camila Campos; McCormick-Barnes, Charlie; See, Pao Theen; Oliver, Richard P.; Moffat, Caroline S.; Cockram, James

doi:10.1007/s00122-019-03517-8

Cited by 29 publications

(25 citation statements)

References 78 publications

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“…For the two proteinaceous toxins, ToxA reacts with a corresponding susceptibility gene in wheat ( Tsn1 ), which makes the host sensitive to the effector [ 7 ], while the corresponding host gene for ToxB remains as yet unknown but is associated with the Tsc2 locus on chromosome 2B [ 8 ].…”

Section: Introductionmentioning

confidence: 99%

PacBio genome sequencing reveals new insights into the genomic organisation of the multi-copy ToxB gene of the wheat fungal pathogen Pyrenophora tritici-repentis

2020

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Background Necrotrophic effector proteins secreted by fungal pathogens are important virulence factors that mediate the development of disease in wheat. Pyrenophora tritici-repentis (Ptr), the causal agent of wheat tan spot, has a race structure dependent on the combination of effectors. In Ptr, ToxA and ToxB are known proteinaceous effectors responsible for necrosis and chlorosis respectively. While Ptr ToxA is encoded by the single gene ToxA, ToxB has multiple loci in the Ptr genome, which is postulated to be directly related to the level of ToxB production and leaf chlorosis. Although previous analysis has indicated that the majority of the ToxB loci lie on a single chromosome, the exact number and chromosomal locations for all the ToxB loci have not been fully identified. Results In this study, we have sequenced the genome of a race 5 ToxB-producing isolate (DW5), using PacBio long read technology, and found that ToxB duplications are nested in the complex subtelomeric chromosomal regions. A total of ten identical ToxB gene copies were identified and based on flanking sequence identity, nine loci appeared associated with chromosome 10 and a single copy with chromosome 5. Chromosome 10 multiple ToxB gene loci were separated by large sequence regions between 31 and 66 kb within larger segmental duplications in an alternating pattern related to loci strand, and flanked by transposable elements. Conclusion This work provides for the first time the full accompaniment of ToxB loci and surrounding regions, and identifies the organization and distribution of ten ToxB loci to subtelomeric regions. To our knowledge, this is the first report of an interwoven strand-related duplication pattern event. This study further highlights the importance of resolving the highly complex distal chromosomal regions, that remain difficult to assemble, and can harbour important effectors and virulence factors.

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Section: Introductionmentioning

confidence: 99%

PacBio genome sequencing reveals new insights into the genomic organisation of the multi-copy ToxB gene of the wheat fungal pathogen Pyrenophora tritici-repentis

2020

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“…PtrToxA is a fibronectin type III-like peptide with an arginyl-glycyl-aspartic acid motif that interacts with Tsn1, a nucleotide-binding site leucine-rich repeat (NBS-LRR) domain and a serine/threonine protein kinase (S/TPK) domain protein. PtrToxB is a cysteine rich, apoplastic toxin, that interacts with the product of the Tsc2 gene in ToxB-sensitive wheat cultivars ( Ciuffetti et al., 2010 ; Figueroa et al., 2015 ; Corsi et al., 2020 ). Several of the candidate effectors identified in the present study were reported by Guyon et al.…”

Section: Discussionmentioning

confidence: 99%

Receptor-Like Kinases BAK1 and SOBIR1 Are Required for Necrotizing Activity of a Novel Group of Sclerotinia sclerotiorum Necrosis-Inducing Effectors

et al. 2020

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Sclerotinia sclerotiorum is a characteristic necrotrophic plant pathogen and is dependent on the induction of host cell death for nutrient acquisition. To identify necrosis-inducing effectors, the genome of S. sclerotiorum was scanned for genes encoding small, secreted, cysteine-rich proteins. These potential effectors were tested for their ability to induce necrosis in Nicotiana benthamiana via Agrobacterium -mediated expression and for cellular localization in host cells. Six novel proteins were discovered, of which all but one required a signal peptide for export to the apoplast for necrotizing activity. Virus-induced gene silencing revealed that the five necrosis-inducing effectors with a requirement for secretion also required the plant co-receptor-like kinases Brassinosteroid Insensitive 1-Associated Receptor Kinase 1 (BAK1) and Suppressor of BAK1-Interacting Receptor-like Kinase 1 (SOBIR1) for the induction of necrosis. S. sclerotiorum necrosis-inducing effector 2 (SsNE2) represented a new class of necrosis-inducing proteins as orthologs were identified in several other phytopathogenic fungi that were also capable of inducing necrosis. Substitution of conserved cysteine residues with alanine reduced, but did not abolish, the necrotizing activity of SsNE2 and full-length protein was required for function as peptides spanning the entire protein were unable to induce necrosis. These results illustrate the importance of necrosis-inducing effectors for S. sclerotiorum virulence and the role of host extracellular receptor(s) in effector-triggered susceptibility to this pathogen.

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“…Different wheat MAGIC populations have been exploited to identify QTL controlling resistance against fungal diseases such as powdery mildew (caused by Blumeria graminis), STB, tan spot (caused by Pyrenophora tritici-repentis) [59,60], and Septoria leaf and glume blotch (caused by Parastagonospora nodorum) [61]. While genetic resistance to STB has been previously identified using BMWpop [60], the phenotypic response was observed under artificial inoculation.…”

Section: Introductionmentioning

confidence: 99%

Genetic Analysis Using a Multi-Parent Wheat Population Identifies Novel Sources of Septoria Tritici Blotch Resistance

Riaz

Kock-Appelgren

Hehir

et al. 2020

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Zymoseptoria tritici is the causative fungal pathogen of septoria tritici blotch (STB) disease of wheat (Triticum aestivum L.) that continuously threatens wheat crops in Ireland and throughout Europe. Under favorable conditions, STB can cause up to 50% yield losses if left untreated. STB is commonly controlled with fungicides; however, a combination of Z. tritici populations developing fungicide resistance and increased restrictions on fungicide use in the EU has led to farmers relying on fewer active substances. Consequently, this serves to drive the emergence of Z. tritici resistance against the remaining chemistries. In response, the use of resistant wheat varieties provides a more sustainable disease management strategy. However, the number of varieties offering an adequate level of resistance against STB is limited. Therefore, new sources of resistance or improved stacking of existing resistance loci are needed to develop varieties with superior agronomic performance. Here, we identified quantitative trait loci (QTL) for STB resistance in the eight-founder “NIAB Elite MAGIC” winter wheat population. The population was screened for STB response in the field under natural infection for three seasons from 2016 to 2018. Twenty-five QTL associated with STB resistance were identified in total. QTL either co-located with previously reported QTL or represent new loci underpinning STB resistance. The genomic regions identified and the linked genetic markers serve as useful resources for STB resistance breeding, supporting rapid selection of favorable alleles for the breeding of new wheat cultivars with improved STB resistance.

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Genetic analysis of wheat sensitivity to the ToxB fungal effector from Pyrenophora tritici-repentis, the causal agent of tan spot

Cited by 29 publications

References 78 publications

PacBio genome sequencing reveals new insights into the genomic organisation of the multi-copy ToxB gene of the wheat fungal pathogen Pyrenophora tritici-repentis

PacBio genome sequencing reveals new insights into the genomic organisation of the multi-copy ToxB gene of the wheat fungal pathogen Pyrenophora tritici-repentis

Receptor-Like Kinases BAK1 and SOBIR1 Are Required for Necrotizing Activity of a Novel Group of Sclerotinia sclerotiorum Necrosis-Inducing Effectors

Genetic Analysis Using a Multi-Parent Wheat Population Identifies Novel Sources of Septoria Tritici Blotch Resistance

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