Carbon acquisition and metabolism changes during fungal biotrophic plant pathogenesis: insights from <i>Ustilago maydis</i>

Abstract

Throughout the plant disease cycle, biotrophic fungal pathogens must obtain host-derived carbon molecules to act as building blocks and sources of energy. Gaining access to these resources requires biotrophic fungi to breach plant cell walls without eliciting substantial plant defences. The plant cell wall is composed mostly of glucose- and xylose-based polysaccharides, which can support fungal growth. Thus, fungi can acquire carbon compounds through the targeted depolymerization of specific wall components. When the plant cell wall is breached, biotrophs redirect photoassimilates, increase sink strengths, and express invertases and transporters to acquire carbon compounds. Transitions in enzyme and transporter expression during pathogenesis must be tightly controlled to ensure a continued supply of carbon compounds. This review describes carbon acquisition and metabolism, including regulation of available carbon source utilization mechanisms such as carbon catabolite repression. While carbon acquisition has been extensively studied in the ascomycetes, the mechanisms used by biotrophic fungi to acquire carbon during pathogenesis are poorly understood. Furthermore, the relationship between plant cell wall-degrading enzymes and carbon acquisition in biotrophic fungal pathogens is not well characterized. As such, this review summarizes the current knowledge of carbon source utilization by fungal pathogens, with an emphasis on research involving the corn smut pathogen Ustilago maydis, and provides a basis from which to extend our knowledge in this key area of fungal plant pathogenesis.