Interaction between the Bird Cherry-Oat Aphid (Rhopalosiphum padi) and Stagonospora Nodorum Blotch (Parastagonospora nodorum) on Wheat

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).

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Volatile molecules secreted by the wheat pathogen Parastagonospora nodorum are involved in development and phytotoxicity

10.1101/729509 ◽

2019 ◽

Cited By ~ 1

Author(s):

M. Jordi Muria-Gonzalez ◽

Hui Yeng Yeannie Yap ◽

Susan Breen ◽

Oliver Mead ◽

Chen Wang ◽

...

Keyword(s):

Mass Spectrometry ◽

Reverse Genetics ◽

Mass Spectrometry Analysis ◽

Synthetic Genes ◽

Spectrometry Analysis ◽

Septoria Nodorum Blotch ◽

Volatile Organic ◽

Wheat Leaves ◽

Plant Assays ◽

Parastagonospora Nodorum

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.

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

10.1101/2021.07.28.454099 ◽

2021 ◽

Author(s):

Evan John ◽

Silke Jacques ◽

Huyen Phan ◽

Lifang Liu ◽

Danilo Pereira ◽

...

Keyword(s):

Regulatory Region ◽

Gene Promoter ◽

Epistatic Effect ◽

Start Codon ◽

Septoria Nodorum Blotch ◽

Trait Locus ◽

Repressor Molecule ◽

Wheat Leaves ◽

Parastagonospora Nodorum ◽

Necrotrophic Effectors

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.

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

PLoS Pathogens ◽

10.1371/journal.ppat.1010149 ◽

2022 ◽

Vol 18 (1) ◽

pp. e1010149

Author(s):

Evan John ◽

Silke Jacques ◽

Huyen T. T. Phan ◽

Lifang Liu ◽

Danilo Pereira ◽

...

Keyword(s):

Regulatory Region ◽

Gene Promoter ◽

Epistatic Effect ◽

Start Codon ◽

Wheat Varieties ◽

Septoria Nodorum Blotch ◽

Trait Locus ◽

Repressor Molecule ◽

Wheat Leaves ◽

Parastagonospora Nodorum

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.

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Advances in genetic mapping of Septoria nodorum blotch resistance in wheat and applications in resistance breeding

10.19103/as.2021.0092.15 ◽

2021 ◽

pp. 393-434

Author(s):

Min Lin ◽

◽

Morten Lillemo ◽

Keyword(s):

Genetic Mapping ◽

Resistance Breeding ◽

Adult Plant ◽

Septoria Nodorum ◽

Septoria Nodorum Blotch ◽

Glume Blotch ◽

Wheat Leaves ◽

Parastagonospora Nodorum

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.

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Specificity of the interaction of TSN1-SnTOXA and SNN1-SnTOX1 genes in the Triticum aestivum - Stagonospora nodorum pathosystem

Biomics ◽

10.31301/2221-6197.bmcs.2020-23 ◽

2020 ◽

Vol 12 (3) ◽

pp. 352-358

Author(s):

T.V. Nuzhnaya ◽

S.V. Veselova ◽

G.F. Burkhanova ◽

S.D. Rumyantsev ◽

I.V. Maksimov

Keyword(s):

Transcriptional Activity ◽

Pathogenic Fungus ◽

Wheat Plant ◽

Wheat Seedling ◽

Susceptibility Genes ◽

Stagonospora Nodorum ◽

Regulation Of Transcription ◽

Wheat Varieties ◽

Seedling Resistance ◽

Septoria Nodorum Blotch

The virulence of the causal agent of Septoria nodorum blotch of wheat pathogenic fungus Stagonospora nodorum Berk. is caused by the presence of necrotrophic effectors (SnTox). Isolates infect wheat varieties that carry susceptibility genes (Snn) corresponding to toxins in the genome. SnTox-Snn interactions are mirror images of classical gene-for-gene interactions and lead to the development of disease. In the present work, we have studied SnTox-Tsn1 and SnTox1-Snn1 interactions resulting in development of necrosis and chlorosis in wheat plant tissues with the formation of extensive lesions. It is assumed that the multiplicity of SnTox-Snn reactions can be carried out through the regulation of transcription of plant susceptibility genes. The aim of the work was to study the transcriptional activity of the Tsn1 and Snn1 susceptibility genes in wheat varieties with varying degrees of resistance to S. nodorum. Alleles of the Tsn1 and Snn1 susceptibility genes were identified by PCR in 12 varieties of winter and spring wheat. Seedling resistance was determined for all samples by the lawns method. Then five varieties were selected for further study. The resistance of the Omskaya 35 variety, which carries a single dominant Snn1 allele, was determined by the suppression of transcription of the Snn1 gene by almost 2 times. The resistance of the Yubileynaya 100 variety, which carries two dominant alleles Tsn1/Snn1, was determined by suppression of transcription of the Tsn1 gene by 8 times. The resistance of the Esaul and Yermak varieties, as well as the susceptibility of the Zhnitsa variety, were determined not only by the transcriptional activity of the Tsn1 gene, but possibly by other factors. A statistically significant positive correlation of 0.97 was found between the transcription level of the Tsn1 gene and the resistance of the variety.

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Co-infection of wheat by Pyrenophora tritici-repentis and Parastagonospora nodorum in the wheatbelt of Western Australia

Crop and Pasture Science ◽

10.1071/cp19412 ◽

2020 ◽

Vol 71 (2) ◽

pp. 119

Author(s):

Araz S. Abdullah ◽

Mark R. Gibberd ◽

John Hamblin

Keyword(s):

Empirical Studies ◽

Triticum Aestivum L ◽

Fungal Species ◽

Tan Spot ◽

Robust Methods ◽

Pyrenophora Tritici Repentis ◽

Septoria Nodorum Blotch ◽

Fungal Abundance ◽

Wheat Leaves ◽

Parastagonospora Nodorum

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.

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Crop infestation by aphids is related to flight activity detected with 75 metre high suction traps

New Zealand Plant Protection ◽

10.30843/nzpp.2004.57.6915 ◽

2004 ◽

Vol 57 ◽

pp. 227-232 ◽

Cited By ~ 5

Author(s):

D.A.J. Teulon ◽

M.A.W. Stufkens ◽

J.D. Fletcher

Keyword(s):

Positive Relationship ◽

Rhopalosiphum Padi ◽

Flight Activity ◽

Aphid Infestation ◽

Potato Aphid ◽

Suction Traps ◽

Suction Trap ◽

Trap Catches ◽

The Relationship ◽

High Suction

The flight activity of aphid pests of wheat potato lettuce and squash is currently monitored in New Zealand using 75 m suction traps However there has been little research comparing aphid suction trap catches with crop infestation levels The relationship between the average number of aphids (Rhopalosiphum padi) sampled from wheat plants and the average number of aphids caught in weekly 75 m suction trap samples was examined A significant positive relationship indicated that numbers of aphids caught in suction traps reflected the numbers of aphids infesting wheat fields In another experiment potato aphid flights (mostly Myzus persicae) caught in a 75 m suction trap were compared with a nearby windvane trap Aphid numbers in both traps reflected similar trends However the suction trap caught approximately 10 times more aphids than the windvane trap Thus 75 m suction traps provide a useful tool for assessing aphid infestation levels in crops

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Epichloë Endophyte-Promoted Seed Pathogen Increases Host Grass Resistance Against Insect Herbivory

Frontiers in Microbiology ◽

10.3389/fmicb.2021.786619 ◽

2022 ◽

Vol 12 ◽

Author(s):

Miika Laihonen ◽

Kari Saikkonen ◽

Marjo Helander ◽

Beatriz R. Vázquez de Aldana ◽

Iñigo Zabalgogeazcoa ◽

...

Keyword(s):

Pathogenic Fungus ◽

Insect Herbivory ◽

Common Garden ◽

Trophic Levels ◽

Context Dependency ◽

Research Station ◽

Natural Setting ◽

Plant Seed ◽

Aphid Infestation ◽

Red Fescue

Plants host taxonomically and functionally complex communities of microbes. However, ecological studies on plant–microbe interactions rarely address the role of multiple co-occurring plant-associated microbes. Here, we contend that plant-associated microbes interact with each other and can have joint consequences for higher trophic levels. In this study we recorded the occurrence of the plant seed pathogenic fungus Claviceps purpurea and aphids (Sitobion sp.) on an established field experiment with red fescue (Festuca rubra) plants symbiotic to a seed transmitted endophytic fungus Epichloë festucae (E+) or non-symbiotic (E–). Both fungi are known to produce animal-toxic alkaloids. The study was conducted in a semi-natural setting, where E+ and E– plants from different origins (Spain and Northern Finland) were planted in a randomized design in a fenced common garden at Kevo Subarctic Research Station in Northern Finland. The results reveal that 45% of E+ plants were infected with Claviceps compared to 31% of E– plants. Uninfected plants had 4.5 times more aphids than Claviceps infected plants. By contrast, aphid infestation was unaffected by Epichloë symbiosis. Claviceps alkaloid concentrations correlated with a decrease in aphid numbers, which indicates their insect deterring features. These results show that plant mutualistic fungi can increase the infection probability of a pathogenic fungus, which then becomes beneficial to the plant by controlling herbivorous insects. Our study highlights the complexity and context dependency of species–species and multi-trophic interactions, thus challenging the labeling of species as plant mutualists or pathogens.

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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.

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Development of SCAR Markers and an SYBR Green Assay to Detect Puccinia striiformis f. sp. tritici in Infected Wheat Leaves

Plant Disease ◽

10.1094/pdis-06-15-0693-re ◽

2016 ◽

Vol 100 (9) ◽

pp. 1840-1847 ◽

Cited By ~ 8

Author(s):

L. Gao ◽

H. X. Yu ◽

X. H. Kang ◽

H. M. Shen ◽

C. Li ◽

...

Keyword(s):

Detection Limit ◽

Puccinia Striiformis ◽

Pathogenic Fungus ◽

Sybr Green ◽

Post Inoculation ◽

Scar Markers ◽

Sequence Characterized Amplified Region ◽

Rust Pathogen ◽

Pcr Method ◽

Wheat Leaves

Stripe rust, caused by the pathogenic fungus Puccinia striiformis f. sp. tritici, is an important disease of wheat worldwide. A rapid and reliable detection of the pathogen in latent infected wheat leaves is useful for accurate and early forecast of outbreaks and timely application of fungicides for managing the disease. Using the previously reported primer pair Bt2a/Bt2b, a 362-bp amplicon was obtained from P. striiformis f. sp. tritici and a 486-bp amplicon was obtained from both P. triticina (the leaf rust pathogen) and P. graminis f. sp. tritici (the stem rust pathogen). Based on the sequence of the 362-bp fragment, two pairs of sequence characterized amplified region (SCAR) primers were designed. PSTF117/PSTR363 produced a 274-bp amplicon and TF114/TR323 produced a 180-bp amplicon from P. striiformis f. sp. tritici, whereas they did not produce any amplicon from P. triticina, P. graminis f. sp. tritici, or any other wheat-infecting fungi. The detection limit of PSTF117/PSTR363 was 1 pg/µl and TF114/TR323 was 100 fg/µl. Both SCAR markers could be detected in wheat leaves 9 h post inoculation. An SYBR Green RT-PCR method was also developed to detect P. striiformis f. sp. tritici in infected leaves with the detection limit of 1.0 fg DNA from asymptomatic leaf samples of 6 h after inoculation. These methods should be useful for rapid diagnosis and accurate detection of P. striiformis f. sp. tritici in infected wheat leaves for timely control of the disease.

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