The rise of necrotrophic effectors

Reactive oxygen species (ROS) play a central role in plant immune responses. The most important virulence factors of the Stagonospora nodorum Berk. are multiple fungal necrotrophic effectors (NEs) (SnTox) that affect the redox-status and cause necrosis and/or chlorosis in wheat lines possessing dominant susceptibility genes (Snn). However, the effect of NEs on ROS generation at the early stages of infection has not been studied. We studied the early stage of infection of various wheat genotypes with S nodorum isolates -Sn4VD, SnB, and Sn9MN, carrying a different set of NE genes. Our results indicate that all three NEs of SnToxA, SnTox1, SnTox3 significantly contributed to cause disease, and the virulence of the isolates depended on their differential expression in plants (Triticum aestivum L.). The Tsn1–SnToxA, Snn1–SnTox1and Snn3–SnTox3 interactions played an important role in inhibition ROS production at the initial stage of infection. The Snn3–SnTox3 inhibited ROS production in wheat by affecting NADPH-oxidases, peroxidases, superoxide dismutase and catalase. The Tsn1–SnToxA inhibited ROS production in wheat by affecting peroxidases and catalase. The Snn1–SnTox1 inhibited the production of ROS in wheat by mainly affecting a peroxidase. Collectively, these results show that the inverse gene-for gene interactions between effector of pathogen and product of host sensitivity gene suppress the host’s own PAMP-triggered immunity pathway, resulting in NE-triggered susceptibility (NETS). These results are fundamentally changing our understanding of the development of this economical important wheat disease.

Download Full-text

Characterizing Virulence of the Pyrenophora tritici-repentis Isolates Lacking Both ToxA and ToxB Genes

Pathogens ◽

10.3390/pathogens7030074 ◽

2018 ◽

Vol 7 (3) ◽

pp. 74 ◽

Cited By ~ 2

Author(s):

Jingwei Guo ◽

Gongjun Shi ◽

Zhaohui Liu

Keyword(s):

Triticum Aestivum L ◽

Tan Spot ◽

Pyrenophora Tritici Repentis ◽

Tan Spot Disease ◽

Hard Red Winter Wheat ◽

Winter Wheat Cultivars ◽

Race 2 ◽

Genomic Regions ◽

Race 4 ◽

Necrotrophic Effectors

The fungus Pyrenophora tritici-repentis (Ptr) causes tan spot of wheat crops, which is an important disease worldwide. Based on the production of the three known necrotrophic effectors (NEs), the fungal isolates are classified into eight races with race 4 producing no known NEs. From a laboratory cross between 86–124 (race 2 carrying the ToxA gene for the production of Ptr ToxA) and DW5 (race 5 carrying the ToxB gene for the production of Ptr ToxB), we have obtained some Ptr isolates lacking both the ToxA and ToxB genes, which, by definition, should be classified as race 4. In this work, we characterized virulence of two of these isolates called B16 and B17 by inoculating them onto various common wheat (Triticum aestivum L.) and durum (T. turgidum L.) genotypes. It was found that the two isolates still caused disease on some genotypes of both common and durum wheat. Disease evaluations were also conducted in recombinant inbred line populations derived from two hard red winter wheat cultivars: Harry and Wesley. QTL mapping in this population revealed that three genomic regions were significantly associated with disease, which are different from the three known NE sensitivity loci. This result further indicates the existence of other NE-host sensitivity gene interactions in the wheat tan spot disease system.

Download Full-text

Absence of detectable yield penalty associated with insensitivity to Pleosporales necrotrophic effectors in wheat grown in the West Australian wheat belt

Plant Pathology ◽

10.1111/ppa.12191 ◽

2014 ◽

Vol 63 (5) ◽

pp. 1027-1032 ◽

Cited By ~ 10

Author(s):

R. Oliver ◽

J. Lichtenzveig ◽

K.-C. Tan ◽

O. Waters ◽

K. Rybak ◽

...

Keyword(s):

The West ◽

Australian Wheat ◽

Necrotrophic Effectors ◽

Yield Penalty

Download Full-text

Parastagonospora nodorum and Related Species in Western Canada: Genetic Variability and Effector Genes

Phytopathology ◽

10.1094/phyto-05-20-0207-r ◽

2020 ◽

Vol 110 (12) ◽

pp. 1946-1958

Author(s):

Mohamed Hafez ◽

Ryan Gourlie ◽

Therese Despins ◽

Thomas K. Turkington ◽

Timothy L. Friesen ◽

...

Keyword(s):

Evolutionary Relationship ◽

Haplotype Network ◽

Bipolaris Sorokiniana ◽

Western Canada ◽

Pyrenophora Tritici Repentis ◽

Septoria Nodorum Blotch ◽

Effector Genes ◽

Parastagonospora Nodorum ◽

Almost All ◽

Necrotrophic Effectors

Parastagonospora nodorum is an important fungal pathogen that causes Septoria nodorum blotch (SNB) in wheat. This pathogen produces several necrotrophic effectors that act as virulence factors; three have been cloned, SnToxA, SnTox1, and SnTox3. In this study, P. nodorum and its sister species P. avenaria f. tritici (Pat1) were isolated from wheat node and grain samples collected from distanced sites in western Canada during 2018. The presence of effector genes and associated haplotypes were determined by PCR and sequence analysis. An internal transcribed spacer-restriction fragment length polymorphism test was developed to distinguish between leaf spotting pathogens (P. nodorum, Pat1, Pyrenophora tritici-repentis, and Bipolaris sorokiniana). P. nodorum was mainly recovered from wheat nodes and to a lesser extent from the grains, while Pat1 was exclusively isolated from grain samples. The effector genes were present in almost all P. nodorum isolates, with the ToxA haplotype 5 (H5) being most prevalent, while a novel ToxA haplotype (denoted here H21) is reported for the first time. In Pat1, only combinations of SnTox1 and SnTox3 genes were present. A ToxA haplotype network was also constructed to assess the evolutionary relationship among globally found haplotypes to date. Finally, cultivars representing wheat development in Canada for the last century were tested for sensitivity to Sn-effectors and to the presence of Tsn1, the ToxA sensitivity gene. Of tested cultivars, 32.9 and 56.9% were sensitive to SnTox1 and SnTox3, respectively, and Tsn1 was present in 59% of the cultivars. In conclusion, P. nodorum and Pat1 were prevalent wheat pathogens in Canada with a potential tissue-specific colonization capacity, while producing necrotrophic effectors to which wheat is sensitive.

Download Full-text

Functional characterization of Stagonospora nodorum necrotrophic effectors

10.18699/icg-plantgen2019-21 ◽

2019 ◽

Keyword(s):

Functional Characterization ◽

Stagonospora Nodorum ◽

Necrotrophic Effectors

Download Full-text

Virulence of Pyrenophora tritici-repentis: a minireview

10.22616/rrd.27.2021.003 ◽

2021 ◽

Author(s):

Janis Kaneps ◽

◽

Biruta Bankina ◽

Inga Moročko-Bičevska ◽

Keyword(s):

Single Copy ◽

Host Susceptibility ◽

Gene Encoding ◽

Pyrenophora Tritici Repentis ◽

Ptr Toxa ◽

Triticum Spp ◽

Copy Gene ◽

Polar Low ◽

Available Information ◽

Necrotrophic Effectors

Pyrenophora tritici-repentis is a major wheat pathogen in all wheat (Triticum spp.) growing areas worldwide. Up to date, eight P. tritici-repentis races have been described based on chlorosis, necrosis, or both symptoms caused on race differential wheat genotypes: ‘Glenlea’, 6B662, 6B365, and ‘Salamouni’. Symptom development on differential genotypes depends on the interaction of the pathogen’s necrotrophic effectors named Ptr ToxA, Ptr ToxB, and Ptr ToxC with host susceptibility genes. Ptr ToxA is encoded by the single copy gene ToxA and induces necrosis on sensitive wheat cultivars. Ptr ToxB causes chlorosis and is encoded by the multicopy gene ToxB. The Ptr ToxC is the non-proteinaceous, polar, low molecular mass molecule that also induces chlorosis, but up to date, the gene encoding this toxin is unknown. Races producing Ptr ToxA are predominant in the global Ptr population. There are several reports about new putative races of P. tritici-repentis that do not conform with the current race system, so further research is required. This study aims to collect and systematise available information about the virulence and races of P. tritici-repentis.

Download Full-text

Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction

New Phytologist ◽

10.1111/j.1469-8137.2010.03362.x ◽

2010 ◽

Vol 187 (4) ◽

pp. 911-919 ◽

Cited By ~ 125

Author(s):

Lynda M. Ciuffetti ◽

Viola A. Manning ◽

Iovanna Pandelova ◽

Melania Figueroa Betts ◽

J. Patrick Martinez

Keyword(s):

Pyrenophora Tritici Repentis ◽

Ptr Toxa ◽

Necrotrophic Effectors

Download Full-text

Identification and Characterization of the SnTox6-Snn6 Interaction in the Parastagonospora nodorum–Wheat Pathosystem

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-12-14-0396-r ◽

2015 ◽

Vol 28 (5) ◽

pp. 615-625 ◽

Cited By ~ 35

Author(s):

Y. Gao ◽

J. D. Faris ◽

Z. Liu ◽

Y. M. Kim ◽

R. A. Syme ◽

...

Keyword(s):

Disease Development ◽

Host Interaction ◽

Septoria Nodorum Blotch ◽

Polymerase Chain ◽

Trait Locus ◽

Parastagonospora Nodorum ◽

Wheat Lines ◽

Necrotrophic Effectors ◽

Sensitivity Gene

Parastagonospora nodorum is a necrotrophic fungal pathogen that causes Septoria nodorum blotch (SNB) (formerly Stagonospora nodorum blotch) on wheat. P. nodorum produces necrotrophic effectors (NE) that are recognized by dominant host sensitivity gene products resulting in disease development. The NE–host interaction is critical to inducing NE-triggered susceptibility (NETS). To date, seven NE–host sensitivity gene interactions, following an inverse gene-for-gene model, have been identified in the P. nodorum–wheat pathosystem. Here, we used a wheat mapping population that segregated for sensitivity to two previously characterized interactions (SnTox1-Snn1 and SnTox3-Snn3-B1) to identify and characterize a new interaction involving the NE designated SnTox6 and the host sensitivity gene designated Snn6. SnTox6 is a small secreted protein that induces necrosis on wheat lines harboring Snn6. Sensitivity to SnTox6, conferred by Snn6, was light-dependent and was shown to underlie a major disease susceptibility quantitative trait locus (QTL). No other QTL were identified, even though the P. nodorum isolate used in this study harbored both the SnTox1 and SnTox3 genes. Reverse transcription-polymerase chain reaction showed that the expression of SnTox1 was not detectable, whereas SnTox3 was expressed and, yet, did not play a significant role in disease development. This work expands our knowledge of the wheat–P. nodorum interaction and further establishes this system as a model for necrotrophic specialist pathosystems.

Download Full-text

Genes Conferring Sensitivity to Stagonospora nodorum Necrotrophic Effectors in Stagonospora Nodorum Blotch-Susceptible U.S. Wheat Cultivars

Plant Disease ◽

10.1094/pdis-08-13-0820-re ◽

2014 ◽

Vol 98 (6) ◽

pp. 746-753 ◽

Cited By ~ 6

Author(s):

Matthew Bertucci ◽

Gina Brown-Guedira ◽

J. Paul Murphy ◽

Christina Cowger

Keyword(s):

United States ◽

Southeastern United States ◽

Stagonospora Nodorum ◽

Wheat Cultivars ◽

Perfect Agreement ◽

Stagonospora Nodorum Blotch ◽

Diagnostic Potential ◽

Moderately Resistant ◽

Necrotrophic Effectors ◽

Sensitivity Gene

Stagonospora nodorum is a necrotrophic fungal pathogen that causes Stagonospora nodorum blotch (SNB), a yield- and quality-reducing disease of wheat. S. nodorum produces a set of necrotrophic effectors (NEs) that interact with the products of host sensitivity genes to cause cell death and increased susceptibility to disease. The focus of this study was determination of NE sensitivity among 25 winter wheat cultivars, many of them from the southeastern United States, that are susceptible to SNB, as well as the moderately resistant ‘NC-Neuse’. Thirty-three isolates of S. nodorum previously collected from seven southeastern U.S. states were cultured for NE production, and the culture filtrates were used in an infiltration bioassay. Control strains of Pichia pastoris that expressed SnToxA, SnTox1, or SnTox3 were also used. All SNB-susceptible cultivars were sensitive to at least one NE, while NC-Neuse was insensitive to all NEs tested. Among the sensitive lines, 32% contained sensitivity gene Tsn1 and 64% contained sensitivity gene Snn3. None were sensitive to SnTox1. Additionally, 10 molecular markers for sensitivity genes Tsn1, Snn1, Snn2, and Snn3 were evaluated for diagnostic potential. Only the marker Xfcp623 for Tsn1 was diagnostic, and it was in perfect agreement with the results of the infiltration bioassays. The results illuminate which NE sensitivity genes may be of concern in breeding for resistance to SNB in the southeastern United States.

Download Full-text

Proteinaceous necrotrophic effectors in fungal virulence

Functional Plant Biology ◽

10.1071/fp10067 ◽

2010 ◽

Vol 37 (10) ◽

pp. 907 ◽

Cited By ~ 47

Author(s):

Kar-Chun Tan ◽

Richard P. Oliver ◽

Peter S. Solomon ◽

Caroline S. Moffat

Keyword(s):

Fungal Pathogens ◽

Host Plants ◽

Triticum Aestivum L ◽

Effector Proteins ◽

Fungal Virulence ◽

Pyrenophora Tritici Repentis ◽

Necrotrophic Fungi ◽

Necrotrophic Effectors ◽

Inside Out ◽

Shed Light

The host–pathogen interface can be considered as a biological battlefront. Molecules produced by both the pathogen and the host are critical factors determining the outcome of the interaction. Recent studies have revealed that an increasing number of necrotrophic fungal pathogens produce small proteinaceous effectors that are able to function as virulence factors. These molecules can cause tissue death in host plants that possess dominant sensitivity genes, leading to subsequent pathogen colonisation. Such effectors are only found in necrotrophic fungi, yet their roles in virulence are poorly understood. However, several recent key studies of necrotrophic effectors from two wheat (Triticum aestivum L.) pathogens, Pyrenophora tritici-repentis (Died.) Drechs. and Stagonospora nodorum (Berk.) Castell. & Germano, have shed light upon how these effector proteins serve to disable the host from the inside out.

Download Full-text