Mitogen-Activated Protein Kinase Signaling in Plant-Interacting Fungi: Distinct Messages from Conserved Messengers

Abstract

Mitogen-activated protein kinases (MAPKs) are evolutionarily conserved proteins that function as key signal transduction components in fungi, plants, and mammals. During interaction between phytopathogenic fungi and plants, fungal MAPKs help to promote mechanical and/or enzymatic penetration of host tissues, while plant MAPKs are required for activation of plant immunity. However, new insights suggest that MAPK cascades in both organisms do not operate independently but that they mutually contribute to a highly interconnected molecular dialogue between the plant and the fungus. As a result, some pathogenesis-related processes controlled by fungal MAPKs lead to the activation of plant signaling, including the recruitment of plant MAPK cascades. Conversely, plant MAPKs promote defense mechanisms that threaten the survival of fungal cells, leading to a stress response mediated in part by fungal MAPK cascades. In this review, we make use of the genomic data available following completion of whole-genome sequencing projects to analyze the structure of MAPK protein families in 24 fungal taxa, including both plant pathogens and mycorrhizal symbionts. Based on conserved patterns of sequence diversification, we also propose the adoption of a unified fungal MAPK nomenclature derived from that established for the model species Saccharomyces cerevisiae. Finally, we summarize current knowledge of the functions of MAPK cascades in phytopathogenic fungi and highlight the central role played by MAPK signaling during the molecular dialogue between plants and invading fungal pathogens.

Distinct and Redundant Roles of Protein Tyrosine Phosphatases Ptp1 and Ptp2 in Governing the Differentiation and Pathogenicity of Cryptococcus neoformans

“…In fungal pathogens, MAPK signaling pathways also play key roles in controlling fungal pathogenicity (6,7). For example, in Cryptococcus neoformans, which causes often-fatal meningoencephalitis in humans (8,9), three MAPKs, including Cpk1, Hog1, and Mpk1, have been found to play pivotal roles in diverse biological events (10,11).…”

Fungal sensing of host environment

“…In fungal pathogens, MAPK signalling, along with the cAMP-PKA pathway, is involved in control of pheromone-and virulence-induced genes (Hamel et al, 2012). The Hog1 pathway is important for response to different stresses in fungi, and furthermore, mediates key functions such as cell-cycle progression, sexual reproduction and morphological differentiation.…”

“…In return, the host induces its own MAPK signalling, in response to recognition of different fungi to either mediate an immune response or tolerance, in terms of a symbiotic or commensal relationship. While it is accepted that in plants, MAPK signalling is used for a molecular dialogue between the plant and the fungi (Hamel et al, 2012;Meng and Zhang, 2013); also, crosstalk between mammals and fungi is mediated via MAPK signalling. In this context, human oral epithelial cells can distinguish C. albicans yeast from hyphal cells and subsequently activate distinct MAPK pathways (Moyes et al, 2010).…”

Molecular characterization of a Hog1-type MAPK, MlpHog1, from Melampsora larici-populina

“…Mitogen-activated protein kinase (MAPK) cascades function as key signal transducers that use protein phosphorylation/dephosphorylation cycles to disseminate information among evolutionarily conserved pathways (Hamel et al 2012). In general, MAPK cascades in eukaryotes consist of three interlinked protein kinases (PKs) activated sequentially (Widmann et al 1999) and different conserved MAPK signalling pathways are used by eukaryotic organisms to control gene expression, differentiation, cell survival, and apoptosis in response to diverse extracellular triggers (Herskowitz 1995;Treisman 1996).…”