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Differential effector gene expression underpins epistasis in a plant fungal disease.

ABSTRACT: Fungal effector-host sensitivity gene interactions play a key role in determining the outcome of septoria nodorum blotch disease (SNB) caused by Parastagonospora nodorum on wheat. The pathosystem is complex and mediated by interaction of multiple fungal necrotrophic effector-host sensitivity gene systems. Three effector sensitivity gene systems are well characterized in this pathosystem; SnToxA-Tsn1, SnTox1-Snn1 and SnTox3-Snn3. We tested a wheat mapping population that segregated for Snn1 and Snn3 with SN15, an aggressive P. nodorum isolate that produces SnToxA, SnTox1 and SnTox3, to study the inheritance of sensitivity to SnTox1 and SnTox3 and disease susceptibility. Interval quantitative trait locus (QTL) mapping showed that the SnTox1-Snn1 interaction was paramount in SNB development on both seedlings and adult plants. No effect of the SnTox3-Snn3 interaction was observed under SN15 infection. The SnTox3-Snn3 interaction was however, detected in a strain of SN15 in which SnTox1 had been deleted (tox1-6). Gene expression analysis indicates increased SnTox3 expression in tox1-6 compared with SN15. This indicates that the failure to detect the SnTox3-Snn3 interaction in SN15 is due - at least in part - to suppressed expression of SnTox3 mediated by SnTox1. Furthermore, infection of the mapping population with a strain deleted in SnToxA, SnTox1 and SnTox3 (toxa13) unmasked a significant SNB QTL on 2DS where the SnTox2 effector sensitivity gene, Snn2, is located. This QTL was not observed in SN15 and tox1-6 infections and thus suggesting that SnToxA and/or SnTox3 were epistatic. Additional QTLs responding to SNB and effectors sensitivity were detected on 2AS1 and 3AL.

SUBMITTER: Phan HT

PROVIDER: S-EPMC5053286 | biostudies-literature | 2016 Aug

REPOSITORIES: biostudies-literature

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Differential effector gene expression underpins epistasis in a plant fungal disease.

Phan Huyen T T HT Rybak Kasia K Furuki Eiko E Breen Susan S Solomon Peter S PS Oliver Richard P RP Tan Kar-Chun KC

The Plant journal : for cell and molecular biology 20160707 4

Fungal effector-host sensitivity gene interactions play a key role in determining the outcome of septoria nodorum blotch disease (SNB) caused by Parastagonospora nodorum on wheat. The pathosystem is complex and mediated by interaction of multiple fungal necrotrophic effector-host sensitivity gene systems. Three effector sensitivity gene systems are well characterized in this pathosystem; SnToxA-Tsn1, SnTox1-Snn1 and SnTox3-Snn3. We tested a wheat mapping population that segregated for Snn1 and S ...[more]

PMID: 27133896

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Project description: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.

Project description:Effector proteins are secreted by plant pathogens to enable host colonization. Typically, effector genes are tightly regulated, have very low expression levels in axenic conditions, and are strongly induced during host colonization. Chromatin remodeling contributes to the activation of effector genes in planta by still poorly known mechanisms. In this work, we investigated the role of histone acetylation in effector gene derepression in plant pathogens. We used Zymoseptoria tritici, a major pathogen of wheat, as a model to determine the role of lysine acetyltransferases (KATs) in plant infection. We showed that effector gene activation is associated with chromatin remodeling, featuring increased acetylation levels of histone H3 lysine 9 (H3K9) and 14 (H3K14) in effector loci. We functionally characterized the role of Z. tritici KATs and demonstrated their distinct contributions to growth, development, and infection. Sas3 is required for host colonization and pycnidia production and is involved in the acetylation of H3K9 and H3K14 in effector loci and, consequently, in effector gene activation during plant infection. We propose that Sas3-mediated histone acetylation is required for the spatiotemporal activation of effector genes and the virulence of Z. tritici. IMPORTANCE Pathogen infections require the production of effectors that enable host colonization. Effectors have diverse functions and are only expressed at certain stages of the infection cycle. Thus, effector genes are tightly regulated by several mechanisms, including chromatin remodeling. Here, we investigate the role of histone acetylation in effector gene activation in the fungal wheat pathogen Zymoseptoria tritici. We demonstrate that lysine acetyltransferases (KATs) are essential for the spatiotemporal regulation of effector genes. We show that the KAT Sas3 is involved in leaf symptom development and pycnidia formation. Importantly, our results indicate that Sas3 controls histone acetylation of effector loci and is a regulator of effector gene activation during stomatal penetration. Overall, our work demonstrates the key role of histone acetylation in regulating gene expression associated with plant infection.

Project description:Effector proteins play crucial roles in determining the outcome of various plant-parasite interactions. Aphids inject salivary effector proteins into plants to facilitate phloem feeding, but some proteins might trigger defense responses in certain plants. The pea aphid, Acyrthosiphon pisum, forms multiple biotypes, and each biotype is specialized to feed on a small number of closely related legume species. Interestingly, all the previously identified biotypes can feed on Vicia faba; hence, it serves as a universal host plant of A. pisum. We hypothesized that the salivary effector proteins have a key role in determining the compatibility between specific host species and A. pisum biotypes and that each biotype produces saliva containing a specific mixture of effector proteins due to differential expression of encoding genes. As the first step to address these hypotheses, we conducted two sets of RNA-seq experiments. RNA-seq analysis of dissected salivary glands (SGs) from reference alfalfa- and pea-specialized A. pisum lines revealed common and line-specific repertoires of candidate salivary effector genes. Based on the results, we created an extended catalogue of A. pisum salivary effector candidates. Next, we used aphid head samples, which contain SGs, to examine biotype-specific expression patterns of candidate salivary genes. RNA-seq analysis of head samples of alfalfa- and pea-specialized biotypes, each represented by three genetically distinct aphid lines reared on either a universal or specific host plant, showed that a majority of the candidate salivary effector genes was expressed in both biotypes at a similar level. Nonetheless, we identified small sets of genes that were differentially regulated in a biotype-specific manner. Little host plant effect (universal vs. specific) was observed on the expression of candidate salivary genes. Analysis of previously obtained genome re-sequenced data of the two biotypes revealed the copy number variations that might explain the differential expression of some candidate salivary genes. In addition, at least four candidate effector genes that were present in the alfalfa biotype but might not be encoded in the pea biotype were identified. This work sets the stage for future functional characterization of candidate genes potentially involved in the determination of plant specificity of pea aphid biotypes.

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Differential effector gene expression underpins epistasis in a plant fungal disease.

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Differential effector gene expression underpins epistasis in a plant fungal disease.

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