scholarly journals Variability in an effector gene promoter of a necrotrophic fungal pathogen dictates epistasis and effector-triggered susceptibility in wheat

2022 ◽  
Vol 18 (1) ◽  
pp. e1010149
Author(s):  
Evan John ◽  
Silke Jacques ◽  
Huyen T. T. Phan ◽  
Lifang Liu ◽  
Danilo Pereira ◽  
...  

The fungus Parastagonospora nodorum uses proteinaceous necrotrophic effectors (NEs) to induce tissue necrosis on wheat leaves during infection, leading to the symptoms of septoria nodorum blotch (SNB). The NEs Tox1 and Tox3 induce necrosis on wheat possessing the dominant susceptibility genes Snn1 and Snn3B1/Snn3D1, respectively. We previously observed that Tox1 is epistatic to the expression of Tox3 and a quantitative trait locus (QTL) on chromosome 2A that contributes to SNB resistance/susceptibility. The expression of Tox1 is significantly higher in the Australian strain SN15 compared to the American strain SN4. Inspection of the Tox1 promoter region revealed a 401 bp promoter genetic element in SN4 positioned 267 bp upstream of the start codon that is absent in SN15, called PE401. Analysis of the world-wide P. nodorum population revealed that a high proportion of Northern Hemisphere isolates possess PE401 whereas the opposite was observed in representative P. nodorum isolates from Australia and South Africa. The presence of PE401 removed the epistatic effect of Tox1 on the contribution of the SNB 2A QTL but not Tox3. PE401 was introduced into the Tox1 promoter regulatory region in SN15 to test for direct regulatory roles. Tox1 expression was markedly reduced in the presence of PE401. This suggests a repressor molecule(s) binds PE401 and inhibits Tox1 transcription. Infection assays also demonstrated that P. nodorum which lacks PE401 is more pathogenic on Snn1 wheat varieties than P. nodorum carrying PE401. An infection competition assay between P. nodorum isogenic strains with and without PE401 indicated that the higher Tox1-expressing strain rescued the reduced virulence of the lower Tox1-expressing strain on Snn1 wheat. Our study demonstrated that Tox1 exhibits both ‘selfish’ and ‘altruistic’ characteristics. This offers an insight into a complex NE-NE interaction that is occurring within the P. nodorum population. The importance of PE401 in breeding for SNB resistance in wheat is discussed.

2021 ◽  
Author(s):  
Evan John ◽  
Silke Jacques ◽  
Huyen Phan ◽  
Lifang Liu ◽  
Danilo Pereira ◽  
...  

The fungus Parastagonospora nodorum uses proteinaceous necrotrophic effectors (NEs) to induce tissue necrosis on wheat leaves during infection, leading to the symptoms of septoria nodorum blotch (SNB). The NEs Tox1 and Tox3 induce necrosis on wheat possessing the dominant susceptibility genes Snn1 and Snn3B1/Snn3D1, respectively. We previously observed that Tox1 is epistatic to the expression of Tox3 and a quantitative trait locus (QTL) on chromosome 2A that contributes to SNB resistance/susceptibility. The expression of Tox1 is significantly higher in the Australian strain SN15 compared to the American strain SN4. Inspection of the Tox1 promoter region revealed a 401 bp promoter genetic element in SN4 positioned 267 bp upstream of the start codon that is absent in SN15, called PE401. Analysis of the world-wide P. nodorum population revealed that a high proportion of Northern Hemisphere isolates possess PE401 whereas the opposite was observed in the Southern Hemisphere. The presence of PE401 ablates the epistatic effect of Tox1 on the contribution of the SNB 2A QTL but not Tox3. PE401 was introduced into the Tox1 promoter regulatory region in SN15 to test for direct regulatory roles. Tox1 expression was markedly reduced in the presence of PE401. This suggests a repressor molecule(s) binds PE401 and inhibits Tox1 transcription. Infection assays also demonstrated that P. nodorum which lacks PE401 is more pathogenic on Snn1 varieties than P. nodorum carrying PE401. An infection competition assay between P. nodorum isogenic strains with and without PE401 indicated that the higher Tox1-expressing strain rescued the reduced virulence of the lower Tox1-expressing strain on Snn1 wheat. Our study demonstrated that Tox1 exhibits both selfish and altruistic characteristics. This offers an insight into a NE arms race that is occurring within the P. nodorum population. The importance of PE401 in breeding for SNB resistance in wheat is discussed.


2019 ◽  
Author(s):  
M. Jordi Muria-Gonzalez ◽  
Hui Yeng Yeannie Yap ◽  
Susan Breen ◽  
Oliver Mead ◽  
Chen Wang ◽  
...  

AbstractSeptoria nodorum blotch is a major disease of wheat caused by the fungus Parastagonospora nodorum. Recent studies have demonstrated that secondary metabolites, including polyketides and non-ribosomal peptides, produced by the pathogen play important roles in disease and development. However, there is currently no knowledge on the composition or biological activity of the volatile organic compounds (VOCs) secreted by P. nodorum. To address this, we undertook a series of growth and phytotoxicity assays and demonstrated that P. nodorum VOCs inhibited bacterial growth, were phytotoxic and suppressed self-growth. Mass spectrometry analysis revealed that 3-methyl-1-butanol, 2-methyl-1-butanol, 2-methyl-1-propanol and 2-phenylethanol were dominant in the VOC mixture and phenotypic assays using these short chain alcohols confirmed that they were phytotoxic. Further analysis of the VOCs also identified the presence of multiple sesquiterpenes of which four were identified via mass spectrometry and nuclear magnetic resonance as β-elemene, α-cyperone, eudesma-4,11-diene and acora-4,9-diene. Subsequent reverse genetics studies were able to link these molecules to corresponding sesquiterpene synthases in the P. nodorum genome. However, despite extensive testing, these molecules were not involved in either of the growth inhibition or phytotoxicity phenotypes previously observed. Plant assays using mutants of the pathogen lacking the synthetic genes revealed that the identified sesquiterpenes were not required for disease formation on wheat leaves. Collectively, these data have significantly extended our knowledge of the VOCs in fungi and provided the basis for further dissecting the roles of sesquiterpenes in plant disease.


2015 ◽  
Vol 28 (5) ◽  
pp. 615-625 ◽  
Author(s):  
Y. Gao ◽  
J. D. Faris ◽  
Z. Liu ◽  
Y. M. Kim ◽  
R. A. Syme ◽  
...  

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.


Insects ◽  
2021 ◽  
Vol 12 (1) ◽  
pp. 35
Author(s):  
Belachew Asalf ◽  
Andrea Ficke ◽  
Ingeborg Klingen

Wheat plants are under constant attack by multiple pests and diseases. Until now, there are no studies on the interaction between the aphid Rhopalosiphum padi and the plant pathogenic fungus Parastagonospora nodorum causal agent of septoria nodorum blotch (SNB) on wheat. Controlled experiments were conducted to determine: (i) The preference and reproduction of aphids on P. nodorum inoculated and non-inoculated wheat plants and (ii) the effect of prior aphid infestation of wheat plants on SNB development. The preference and reproduction of aphids was determined by releasing female aphids on P. nodorum inoculated (SNB+) and non-inoculated (SNB−) wheat leaves. The effect of prior aphid infestation of wheat plants on SNB development was determined by inoculating P. nodorum on aphid-infested (Aphid+) and aphid free (Aphid−) wheat plants. Higher numbers of aphids moved to and settled on the healthy (SNB−) leaves than inoculated (SNB+) leaves, and reproduction was significantly higher on SNB− leaves than on SNB+ leaves. Aphid infestation of wheat plants predisposed the plants to P. nodorum infection and colonization. These results are important to understand the interactions between multiple pests in wheat and hence how to develop new strategies in future integrated pest management (IPM).


2021 ◽  
pp. 393-434
Author(s):  
Min Lin ◽  
◽  
Morten Lillemo ◽  

Septoria nodorum blotch (SNB) caused by the necrotrophic fungus Parastagonospora nodorum is an important wheat disease in many high rainfall areas across the world. It reduces both yield and grain quality by causing symptoms on wheat leaves and glumes, and can cause yield losses up to 30% under warm and humid conditions. This book chapter gives an update on the recent progress in genetic mapping of SNB resistance in wheat, with focus on adult plant leaf blotch and glume blotch resistance with relevance to resistance breeding. This is followed by a case study on the investigation of the naturally occurring P. nodorum population in Norway and mapping of resistance loci in relevant wheat germplasm using MAGIC populations and GWAS panels as well as how this information can be used to improve resistance breeding and disease management. In the end, some future perspectives of SNB resistance breeding is provided.


2020 ◽  
Vol 71 (2) ◽  
pp. 119
Author(s):  
Araz S. Abdullah ◽  
Mark R. Gibberd ◽  
John Hamblin

The pathogenic fungal species Pyrenophora tritici-repentis (Ptr) and Parastagonospora nodorum (Pan) are common in many wheat-producing parts of the world. These two fungi cause tan spot and septoria nodorum blotch, respectively, frequently co-infecting wheat leaves. Empirical studies of this and other co-infections are rare because of the visual similarity of symptoms and the lack of robust methods for quantifying the abundance of pathogens associated with the co-infection. Here, we use a recently developed molecular method that simultaneously distinguishes and quantifies, in DNA equivalent, the abundance of Ptr and Pan, thereby allowing the prevalence of co-infection to be determined. The study examines the prevalence of co-infection under field conditions, at three widely spaced sites and on three wheat (Triticum aestivum L.) cultivars varying in disease resistance. Co-infection by Ptr and Pan was almost ubiquitous (overall prevalence 94%), and Pan DNA was detected only in association with Ptr. Although Ptr and Pan commonly co-infected, Ptr was more abundant during early and mid-season, at 80% of total fungal abundance when crops were tillering and 67% at booting stage. Pan became as abundant as Ptr when crops reached flowering. Variability in total fungal abundance and disease severity was primarily determined by cultivar; however, Ptr was the more abundant despite differences in cultivar resistance to this pathogen.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Jonathan Brassac ◽  
Quddoos H. Muqaddasi ◽  
Jörg Plieske ◽  
Martin W. Ganal ◽  
Marion S. Röder

AbstractTotal spikelet number per spike (TSN) is a major component of spike architecture in wheat (Triticumaestivum L.). A major and consistent quantitative trait locus (QTL) was discovered for TSN in a doubled haploid spring wheat population grown in the field over 4 years. The QTL on chromosome 7B explained up to 20.5% of phenotypic variance. In its physical interval (7B: 6.37–21.67 Mb), the gene FLOWERINGLOCUST (FT-B1) emerged as candidate for the observed effect. In one of the parental lines, FT-B1 carried a non-synonymous substitution on position 19 of the coding sequence. This mutation modifying an aspartic acid (D) into a histidine (H) occurred in a highly conserved position. The mutation was observed with a frequency of ca. 68% in a set of 135 hexaploid wheat varieties and landraces, while it was not found in other plant species. FT-B1 only showed a minor effect on heading and flowering time (FT) which were dominated by a major QTL on chromosome 5A caused by segregation of the vernalization gene VRN-A1. Individuals carrying the FT-B1 allele with amino acid histidine had, on average, a higher number of spikelets (15.1) than individuals with the aspartic acid allele (14.3) independent of their VRN-A1 allele. We show that the effect of TSN is not mainly related to flowering time; however, the duration of pre-anthesis phases may play a major role.


2021 ◽  
Author(s):  
Rodrigo S Reis ◽  
Jules Deforges ◽  
Romy R Schmidt ◽  
Jos H M Schippers ◽  
Yves Poirier

Abstract A large portion of eukaryotic genes are associated with noncoding, natural antisense transcripts (NATs). Despite sharing extensive sequence complementarity with their sense mRNAs, mRNA-NAT pairs elusively often evade dsRNA-cleavage and siRNA-triggered silencing. More surprisingly, some NATs enhance translation of their sense mRNAs by yet unknown mechanism(s). Here we show that translation enhancement of the rice (Oryza sativa) PHOSPHATE1.2 (PHO1.2) mRNA is enabled by specific structural rearrangements guided by its noncoding antisense RNA (cis-NATpho1.2). Their interaction in vitro revealed no evidence of widespread intermolecular dsRNA formation, but rather specific local changes in nucleotide base-pairing, leading to higher flexibility of PHO1.2 mRNA at a key high GC regulatory region inhibiting translation, approximately 350 nucleotides downstream of the start codon. Sense-antisense RNA interaction increased formation of the 80S complex in PHO1.2, possibly by inducing structural rearrangement within this inhibitory region, thus making this mRNA more accessible to 60S. This work presents a framework for nucleotide-resolution studies of functional mRNA-antisense pairs. One-sentence summary: Interaction between PHO1.2 mRNA and its cis-natural antisense transcript enhances translation via a mechanism involving a local conformational shift and disruption of a key inhibitory region.


Author(s):  
Hammad A Khan ◽  
Yukiko Nakamura ◽  
Robert T Furbank ◽  
John R Evans

Abstract A growing number of leaf traits can be estimated from hyperspectral reflectance data. These include structural and compositional traits, such as leaf mass per area (LMA) and nitrogen and chlorophyll content, but also physiological traits such a Rubisco carboxylation activity, electron transport rate, and respiration rate. Since physiological traits vary with leaf temperature, how does this impact on predictions made from reflectance measurements? We investigated this with two wheat varieties, by repeatedly measuring each leaf through a sequence of temperatures imposed by varying the air temperature in a growth room. Leaf temperatures ranging from 20 °C to 35 °C did not alter the estimated Rubisco capacity normalized to 25 °C (Vcmax25), or chlorophyll or nitrogen contents per unit leaf area. Models estimating LMA and Vcmax25/N were both slightly influenced by leaf temperature: estimated LMA increased by 0.27% °C–1 and Vcmax25/N increased by 0.46% °C–1. A model estimating Rubisco activity closely followed variation associated with leaf temperature. Reflectance spectra change with leaf temperature and therefore contain a temperature signal.


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