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Mannitol is required for asexual sporulation in the wheat pathogen Stagonospora nodorum (glume blotch).

ABSTRACT: The physiological role of the mannitol cycle in the wheat pathogen Stagonospora nodorum (glume blotch) has been investigated by reverse genetics and metabolite profiling. A putative mannitol 2-dehydrogenase gene (Mdh1) was cloned by degenerate PCR and disrupted. The resulting mutated mdh1 strains lacked all detectable NADPH-dependent mannitol dehydrogenase activity. The mdh1 strains were unaffected for mannitol production but, surprisingly, were still able to utilize mannitol as a sole carbon source, suggesting a hitherto unknown mechanism for mannitol catabolism. The mutant strains were not compromised in their ability to cause disease or sporulate. To further our understanding of mannitol metabolism, a previously developed mannitol-1-phosphate dehydrogenase (gene mpd1) disruption construct [Solomon, Tan and Oliver (2005) Mol. Plant-Microbe Interact. 18, 110-115] was introduced into the mutated mdh1 background, resulting in a strain lacking both enzyme activities. The mpd1mdh1 strains were unable to grow on mannitol and produced only trace levels of mannitol. The double-mutant strains were unable to sporulate in vitro when grown on minimal medium for extended periods. Deficiency in sporulation was correlated with the depletion of intracellular mannitol pools. Significantly sporulation could be restored with the addition of mannitol. Pathogenicity of the double mutant was not compromised, although, like the previously characterized mpd1 mutants, the strains were unable to sporulate in planta. These findings not only question the currently hypothesized pathways of mannitol metabolism, but also identify for the first time that mannitol is required for sporulation of a filamentous fungus.

SUBMITTER: Solomon PS

PROVIDER: S-EPMC1609904 | biostudies-literature | 2006 Oct

REPOSITORIES: biostudies-literature

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Mannitol is required for asexual sporulation in the wheat pathogen Stagonospora nodorum (glume blotch).

Solomon Peter S PS Waters Ormonde D C OD Jörgens Cordula I CI Lowe Rohan G T RG Rechberger Judith J Trengove Robert D RD Oliver Richard P RP

The Biochemical journal 20061001 2

The physiological role of the mannitol cycle in the wheat pathogen Stagonospora nodorum (glume blotch) has been investigated by reverse genetics and metabolite profiling. A putative mannitol 2-dehydrogenase gene (Mdh1) was cloned by degenerate PCR and disrupted. The resulting mutated mdh1 strains lacked all detectable NADPH-dependent mannitol dehydrogenase activity. The mdh1 strains were unaffected for mannitol production but, surprisingly, were still able to utilize mannitol as a sole carbon so ...[more]

PMID: 16859492

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Project description:BACKGROUND:In the late 1920s, A. E. Watkins collected about 7000 landrace cultivars (LCs) of bread wheat (Triticum aestivum L.) from 32 different countries around the world. Among which 826 LCs remain viable and could be a valuable source of superior/favorable alleles to enhance disease resistance in wheat. In the present study, a core set of 121 LCs, which captures the majority of the genetic diversity of Watkins collection, was evaluated for identifying novel sources of resistance against tan spot, Stagonospora nodorum blotch (SNB), and Fusarium Head Blight (FHB). RESULTS:A diverse response was observed in 121 LCs for all three diseases. The majority of LCs were moderately susceptible to susceptible to tan spot Ptr race 1 (84%) and FHB (96%) whereas a large number of LCs were resistant or moderately resistant against tan spot Ptr race 5 (95%) and SNB (54%). Thirteen LCs were identified in this study could be a valuable source for multiple resistance to tan spot Ptr races 1 and 5, and SNB, and another five LCs could be a potential source for FHB resistance. GWAS analysis was carried out using disease phenotyping score and 8807 SNPs data of 118 LCs, which identified 30 significant marker-trait associations (MTAs) with -log10 (p-value) > 3.0. Ten, five, and five genomic regions were found to be associated with resistance to tan spot Ptr race 1, race 5, and SNB, respectively in this study. In addition to Tsn1, several novel genomic regions Q.Ts1.sdsu-4BS and Q.Ts1.sdsu-5BS (tan spot Ptr race 1) and Q.Ts5.sdsu-1BL, Q.Ts5.sdsu-2DL, Q.Ts5.sdsu-3AL, and Q.Ts5.sdsu-6BL (tan spot Ptr race 5) were also identified. Our results indicate that these putative genomic regions contain several genes that play an important role in plant defense mechanisms. CONCLUSION:Our results suggest the existence of valuable resistant alleles against leaf spot diseases in Watkins LCs. The single-nucleotide polymorphism (SNP) markers linked to the quantitative trait loci (QTLs) for tan spot and SNB resistance along with LCs harboring multiple disease resistance could be useful for future wheat breeding.

Project description:The wheat pathogen Stagonospora nodorum produces multiple necrotrophic effectors (also called host-selective toxins) that promote disease by interacting with corresponding host sensitivity gene products. SnTox1 was the first necrotrophic effector identified in S. nodorum, and was shown to induce necrosis on wheat lines carrying Snn1. Here, we report the molecular cloning and validation of SnTox1 as well as the preliminary characterization of the mechanism underlying the SnTox1-Snn1 interaction which leads to susceptibility. SnTox1 was identified using bioinformatics tools and verified by heterologous expression in Pichia pastoris. SnTox1 encodes a 117 amino acid protein with the first 17 amino acids predicted as a signal peptide, and strikingly, the mature protein contains 16 cysteine residues, a common feature for some avirulence effectors. The transformation of SnTox1 into an avirulent S. nodorum isolate was sufficient to make the strain pathogenic. Additionally, the deletion of SnTox1 in virulent isolates rendered the SnTox1 mutated strains avirulent on the Snn1 differential wheat line. SnTox1 was present in 85% of a global collection of S. nodorum isolates. We identified a total of 11 protein isoforms and found evidence for strong diversifying selection operating on SnTox1. The SnTox1-Snn1 interaction results in an oxidative burst, DNA laddering, and pathogenesis related (PR) gene expression, all hallmarks of a defense response. In the absence of light, the development of SnTox1-induced necrosis and disease symptoms were completely blocked. By comparing the infection processes of a GFP-tagged avirulent isolate and the same isolate transformed with SnTox1, we conclude that SnTox1 may play a critical role during fungal penetration. This research further demonstrates that necrotrophic fungal pathogens utilize small effector proteins to exploit plant resistance pathways for their colonization, which provides important insights into the molecular basis of the wheat-S. nodorum interaction, an emerging model for necrotrophic pathosystems.

Dataset Information

Mannitol is required for asexual sporulation in the wheat pathogen Stagonospora nodorum (glume blotch).

Publications

Mannitol is required for asexual sporulation in the wheat pathogen Stagonospora nodorum (glume blotch).

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