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Molecular Biology and Biochemistry of Plant/Pathogen Interactions

Research in my laboratory is directed at understanding the basic processes that mediate interactions between higher plants and pathogenic fungi. Both plants and pathogens produce a variety of molecules during pathogenesis; our goal is to distinguish between the indispensable and the superfluous components of this complex process.

Successful pathogens need the capacity to penetrate plant surfaces, to colonize plant tissues, and to avoid pre-formed and induced plant resistance factors. Some of the mechanisms by which they do so are non-specific, that is, required by many or all pathogens. Other virulence attributes are highly specific, that is, unique to only certain races or genotypes of pathogen and effective only against a particular type of plant. In the most highly co-evolved plant/pathogen interactions, specificity and virulence are controlled by single, corresponding genes in both the pathogen and the plant.

Many cellular plant pathogens penetrate plant tissues by enzymatic digestion of the polymers of the plant cell wall. Cell-wall-degrading enzymes alsofunction as signals to plants that they are under attack, and plants respond by synthesizing anti-microbial proteins and chemicals. We are studying the multifarious roles of wall degrading enzymes in plant pathogenic fungi using transformation-mediated gene disruption to create mutants that lack specific enzymes such as poly-galacturonase and xylanase. A complementary approach is to identify and mutate genes that regulate enzyme production.

Host-selective toxins are natural products (also known as secondary metabolites) that account for the specificity and high virulence of certain plant pathogenic fungi. Host-selective toxins have been implicated in at least two major crop epidemics in the U.S. Intriguingly, production of host-selective toxins is often under the control of single genetic loci. We have shown that the genetic locus responsible for production of HC-toxin, made by the maize pathogen Cochliobolus carbonum, is in fact a gene cluster, containing at least five individual genes encoding enzymes in the biosynthetic pathway. The central enzyme is a 570-kDa polypeptide encoded by a 16-kb open reading frame. The HC-toxin gene cluster is completely lacking in isolates of C. carbonum that do not make HC-toxin and is on a “dispensable” chromosome. Studies on the origin of the capacity for HC-toxin production are yielding insights into the evolution of pathogenicity.

The biochemical basis of resistance in maize to C. carbonum is an enzyme that detoxifies HC-toxin. The site of action of HC-toxin is histone deacetylase, an enzyme that regulates gene expression via alteration of chromatin structure. We are currently addressing the following questions regarding histone deacetylases in the plant and the fungus: (1) How does inhibition of histone deactylase allow C. carbonum to pathogenize maize? (2) How does C. carbonum protect itself against its own toxin? (3) What is the role of fungal histone deacetylases in pathogenesis?

Selected Publications

Hallen HE, Luo H, Scott-Craig JS, Walton JD (2007) A gene family encoding the major toxins of lethal Amanita mushrooms. Proc Natl Acad Sci USA 104: 19097-19101 [cover article] Abstract

Paper JM, Scott-Craig JS, Adhikari ND, Cuomo CA, Walton JD (2007) Comparative proteomics of extracellular proteins in vitro and in planta from the pathogenic fungus Fusarium graminearum. Proteomics 7: 3171-3183

Walton JD (2006) Molecules of interest: HC-toxin. Phytochemistry 67: 1406-1413

Walton JD, Panaccione DG, Hallen H (2004) Peptide synthesis without ribosomes. In J Tkacz, L Lange, eds, Advances in Fungal Biotechnology for Industry, Agriculture, and Medicine. Kluwer Academic, New York, pp 127-162

Hazen SP, Hawley RM, Davis GL, Henrissat B, Walton JD (2003) Quantitative trait loci and comparative genomics of cereal cell wall composition. Plant Physiol 132: 263-271 Abstract

Baidyaroy D, Brosch G, Ahn J-H, Graessle S, Wegener S, Tonukari NJ, Caballero O, Loidl P, Walton JD (2001) A gene related to yeast HOS2 histone deacetylase affects extracellular depolymerase expression and virulence in a plant pathogenic fungus. Plant Cell 13: 1609-1624 Article

Pedley KF, Walton JD (2001) Regulation of cyclic peptide biosynthesis in a plant pathogenic fungus by a novel transcription factor. Proc Natl Acad Sci USA 98: 14174-14179 (see Commentary, PNAS 98: 14187-14188) Abstract

Walton JD (2000) Horizontal gene transfer and the origin of secondary metabolite gene clusters in fungi: an hypothesis. Fung Genet Biol 30: 167-171

Tonukari NJ, Scott-Craig JS, Walton JD (2000) The Cochliobolus carbonum SNF1 gene is required for cell wall-degrading enzyme expression and virulence on maize. Plant Cell 12: 237-248 Abstract

Cheng Y-Q, Walton JD (2000) A eukaryotic alanine racemase involved in cyclic peptide biosynthesis. J Biol Chem 275: 4906-5004 Abstract

Ransom RF, Walton JD (1997) Histone hyperacetylation in maize in response to treatment with HC-toxin or infection by Cochliobolus carbonum. Plant Physiol 115: 1021-1027 Abstract

Walton JD (1996) Host-selective toxins: agents of compatibility. Plant Cell 8: 1723-1733 Article

Brosch G, Ransom R, Lechner T, Walton JD, Loidl P (1995) Inhibition of maize histone deacetylases by HC toxin, the host-selective toxin of Cochliobolus carbonum.  Plant Cell 7: 1941-1950 Abstract

Walton JD (1994) Deconstructing the cell wall. Plant Physiol 104: 1113-1118 Article

Meeley RM, Johal GS, Briggs SP, Walton JD (1992) A biochemical phenotype for a disease resistance gene of maize. Plant Cell 4: 71-77 Abstract

Scott-Craig JS, Panaccione DG, Pocard JA, Walton JD (1992) The multifunctional cyclic peptide synthetase catalyzing HC-toxin production in the filamentous fungus Cochliobolus carbonum is encoded by a 15.7-kb open reading frame. J Biol Chem 67: 26044-26049 Abstract

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