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Maize susceptibility to Ustilago maydis is influenced by genetic and chemical perturbation of carbohydrate allocation.

ABSTRACT: The ability of biotrophic fungi to metabolically adapt to the host environment is a critical factor in fungal diseases of crop plants. In this study, we analysed the transcriptome of maize tumours induced by Ustilago maydis to identify key features underlying metabolic shifts during disease. Among other metabolic changes, this analysis highlighted modifications during infection in the transcriptional regulation of carbohydrate allocation and starch metabolism. We confirmed the relevance of these changes by establishing that symptom development was altered in an id1 (indeterminate1) mutant that showed increased accumulation of sucrose as well as being defective in the vegetative to reproductive transition. We further established the relevance of specific metabolic functions related to carbohydrate allocation by assaying disease in su1 (sugary1) mutant plants with altered starch metabolism and in plants treated with glucose, sucrose and silver nitrate during infection. We propose that specific regulatory and metabolic changes influence the balance between susceptibility and resistance by altering carbon allocation to promote fungal growth or to influence plant defence. Taken together, these studies reveal key aspects of metabolism that are critical for biotrophic adaptation during the maize-U. maydis interaction.

SUBMITTER: Kretschmer M

PROVIDER: S-EPMC6638311 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Maize susceptibility to Ustilago maydis is influenced by genetic and chemical perturbation of carbohydrate allocation.

Kretschmer Matthias M Croll Daniel D Kronstad James W JW

Molecular plant pathology 20161114 9

The ability of biotrophic fungi to metabolically adapt to the host environment is a critical factor in fungal diseases of crop plants. In this study, we analysed the transcriptome of maize tumours induced by Ustilago maydis to identify key features underlying metabolic shifts during disease. Among other metabolic changes, this analysis highlighted modifications during infection in the transcriptional regulation of carbohydrate allocation and starch metabolism. We confirmed the relevance of these ...[more]

PMID: 27564861

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Project description:Filamentous fungi are keystone microorganisms in the regulation of many processes occurring on Earth, such as plant biomass decay and pathogenesis as well as symbiotic associations. In many of these processes, fungi secrete carbohydrate-active enzymes (CAZymes) to modify and/or degrade carbohydrates. Ten years ago, while evaluating the potential of a secretome from the maize pathogen Ustilago maydis to supplement lignocellulolytic cocktails, we noticed it contained many unknown or poorly characterized CAZymes. Here, and after reannotation of this data set and detailed phylogenetic analyses, we observed that several CAZymes (including glycoside hydrolases and carbohydrate oxidases) are predicted to act on the fungal cell wall (FCW), notably on β-1,3-glucans. We heterologously produced and biochemically characterized two new CAZymes, called UmGH16_1-A and UmAA3_2-A. We show that UmGH16_1-A displays β-1,3-glucanase activity, with a preference for β-1,3-glucans with short β-1,6 substitutions, and UmAA3_2-A is a dehydrogenase catalyzing the oxidation of β-1,3- and β-1,6-gluco-oligosaccharides into the corresponding aldonic acids. Working on model β-1,3-glucans, we show that the linear oligosaccharide products released by UmGH16_1-A are further oxidized by UmAA3_2-A, bringing to light a putative biocatalytic cascade. Interestingly, analysis of available transcriptomics data indicates that both UmGH16_1-A and UmAA3_2-A are coexpressed, only during early stages of U. maydis infection cycle. Altogether, our results suggest that both enzymes are connected and that additional accessory activities still need to be uncovered to fully understand the biocatalytic cascade at play and its physiological role. IMPORTANCE Filamentous fungi play a central regulatory role on Earth, notably in the global carbon cycle. Regardless of their lifestyle, filamentous fungi need to remodel their own cell wall (mostly composed of polysaccharides) to grow and proliferate. To do so, they must secrete a large arsenal of enzymes, most notably carbohydrate-active enzymes (CAZymes). However, research on fungal CAZymes over past decades has mainly focused on finding efficient plant biomass conversion processes while CAZymes directed at the fungus itself have remained little explored. In the present study, using the maize pathogen Ustilago maydis as model, we set off to evaluate the prevalence of CAZymes directed toward the fungal cell wall during growth of the fungus on plant biomass and characterized two new CAZymes active on fungal cell wall components. Our results suggest the existence of a biocatalytic cascade that remains to be fully understood.

Dataset Information

Maize susceptibility to Ustilago maydis is influenced by genetic and chemical perturbation of carbohydrate allocation.

Publications

Maize susceptibility to Ustilago maydis is influenced by genetic and chemical perturbation of carbohydrate allocation.

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