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Conserved requirement for a plant host cell protein in powdery mildew pathogenesis

Abstract

In the fungal phylum Ascomycota, the ability to cause disease in plants and animals has been gained and lost repeatedly during phylogenesis1. In monocotyledonous barley, loss-of-function mlo alleles result in effective immunity against the Ascomycete Blumeria graminis f. sp. hordei, the causal agent of powdery mildew disease2,3. However, mlo-based disease resistance has been considered a barley-specific phenomenon to date. Here, we demonstrate a conserved requirement for MLO proteins in powdery mildew pathogenesis in the dicotyledonous plant species Arabidopsis thaliana. Epistasis analysis showed that mlo resistance in A. thaliana does not involve the signaling molecules ethylene, jasmonic acid or salicylic acid, but requires a syntaxin, glycosyl hydrolase and ABC transporter4,5,6. These findings imply that a common host cell entry mechanism of powdery mildew fungi evolved once and at least 200 million years ago, suggesting that within the Erysiphales (powdery mildews) the ability to cause disease has been a stable trait throughout phylogenesis.

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Figure 1: Loss of AtMLO2 function confers powdery mildew resistance in A. thaliana.
Figure 2: Atmlo2 plants show developmentally controlled callose deposition and early senescence-like phenotypes.
Figure 3: Atmlo2/6/12 mutants show a developmentally controlled increase in salicylic acid levels.
Figure 4: Salicylic acid has a role in the age-related phenotypes of Atmlo2.
Figure 5: Atmlo2-mediated resistance requires components of non-host resistance.

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Acknowledgements

We thank T. Gjetting (Biotechnology Research and Innovation Centre, Denmark) and J. Shrager (Carnegie Institution) for helpful discussions. We acknowledge the Salk Institute, The Sainsbury Laboratory, Syngenta and the Arabidopsis Biological Resource Center for providing T-DNA/transposon insertion lines and some of the mutant lines. This work was supported by grants from the Max-Planck Society and the Deutsche Forschungsgemeinschaft (PA861/4; to R.P.); grants from the US National Science Foundation (0114783 and 0519898) and the Carnegie Institution (to S.C.S.) and a US National Institutes of Health (NIH) fellowship (FG32 GN19499-01 to J.V.).

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Correspondence to Ralph Panstruga.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

AtMLO co-orthologs are required for susceptibility to two powdery mildew species. (PDF 237 kb)

Supplementary Fig. 2

Interactions between Atmlo mutants and nonadapted pathogens. (PDF 74 kb)

Supplementary Fig. 3

Atmlo mutants exhibit constitutively elevated levels of salicylic acid. (PDF 23 kb)

Supplementary Fig. 4

Enhanced powdery mildew host cell entry in Atmlo2 NahG plants is likely due to non-SA-dependent defense responses. (PDF 21 kb)

Supplementary Fig. 5

The PEN2 glycosyl hydrolase is an evolutionarily recent acquisition. (PDF 24 kb)

Supplementary Table 1

Atmlo alleles used in this study. (PDF 48 kb)

Supplementary Table 2

Nucleotide sequences of oligonucleotides used in this study. (PDF 7 kb)

Supplementary Methods (PDF 38 kb)

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Consonni, C., Humphry, M., Hartmann, H. et al. Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat Genet 38, 716–720 (2006). https://doi.org/10.1038/ng1806

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