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Review
. 2012 Apr;24(4):1327-51.
doi: 10.1105/tpc.112.096156. Epub 2012 Apr 18.

Mitogen-activated protein kinase signaling in plant-interacting fungi: distinct messages from conserved messengers

Louis-Philippe Hamel  1 , Marie-Claude Nicole, Sébastien Duplessis, Brian E Ellis
Affiliations
Review

Mitogen-activated protein kinase signaling in plant-interacting fungi: distinct messages from conserved messengers

Louis-Philippe Hamel et al. Plant Cell. 2012 Apr.

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.

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Figures

Figure 1.
Figure 1.
MAPK Pathways in S. cerevisiae. Yeast cells rely on four MAPK cascades to regulate mating, invasive growth, cell integrity, and high osmolarity. Smk1 may be part of a fifth, yet undefined, pathway that regulates ascospore formation. Activation of MAPK cascades depends on transmembrane receptors that perceive extracellular cues and translate information to intracellular signaling components, including GTPases, GEFs, and PKs. Upstream regulators may be shared between distinct signaling pathways, and timely activation of a specific cascade must be tightly regulated. In some cases, signal specificity is achieved through the use of scaffolding proteins promoting interaction between suitable MAPK signaling components. Following activation, MAPKs phosphorylate an array of substrates, including TFs that induce a transcriptional shift controlling output responses. See text for more details on each signaling pathway. In light of this study, the acronym “Sce” (for S. cerevisiae) was added to the standard nomenclature of yeast MAPKs.
Figure 2.
Figure 2.
Phylogenetic Relationships of MAPKs from Plant-Interacting Fungi. Genome assembly from various fungi was searched using amino acid sequence of yeast MAPKs as queries. Retrieved gene models were accepted only if corresponding protein displayed consensus sequences of Ser/Thr PKs, including conserved Asp and Lys residues within the active site (D[L/I/V]K motif), and an appropriately positioned activation loop comprising the conserved -TXY- phosphorylation motif. Full-length PKs were next aligned with ClustalW (see Supplemental Data Set 4 online) using plant MAPK At-MPK3 as an outgroup. The following alignment parameters were used: for pairwise alignment, gap opening, 10.0, and gap extension, 0.1; for multiple alignment, gap opening, 10.0, and gap extension, 0.20. Resulting alignments were submitted to Molecular Evolutionary Genetics Analysis 4 (MEGA4) software (Tamura et al., 2007) to generate a neighbor-joining tree derived from 5000 replicates. Bootstrap values are indicated on the nodes of each branch. A colored circle depicts each type of MAPKs, and a species acronym indicates the origin of each protein (Table 1; see Supplemental Data Set 1 online). In relevant cases, previous MAPK nomenclature is indicated in parenthesis.
Figure 3.
Figure 3.
Phylogenetic Relationships of MAP2Ks from Plant-Interacting Fungi. Genome assembly from various fungi was searched using amino acid sequence of yeast MAP2Ks as queries. Retrieved gene models were accepted only if corresponding protein contained consensus sequences of dual-specificity PKs, including conserved Asp and Lys residues within the active site (D[L/I/V]K motif), and an appropriately positioned activation loop comprising the conserved [S/T]xxx[S/T] phosphorylation motif. Full-length PKs were next aligned with ClustalW (see Supplemental Data Set 5 online) using plant MAP2K At-MKK5 as an outgroup. The following alignment parameters were used: for pairwise alignment, gap opening, 10.0, and gap extension, 0.1; for multiple alignment, gap opening, 10.0, and gap extension, 0.20. Resulting alignments were submitted to MEGA4 software to generate a neighbor-joining tree derived from 5000 replicates. Bootstrap values are indicated on the nodes of each branch. A colored circle depicts each type of MAP2K and a species acronym indicates the origin of each protein (Table 1; see Supplemental Data Set 2 online). In relevant cases, previous MAP2K nomenclature is indicated in parenthesis.
Figure 4.
Figure 4.
Phylogenetic Relationships of MAP3Ks from Plant-Interacting Fungi. Genome assembly from various fungi was searched using amino acid sequence of yeast MAP3Ks as queries. Retrieved gene models were accepted only if corresponding protein contained consensus sequences for Ser/Thr PKs, including conserved Asp and Lys residues within the active site (D[L/I/V]K motif). Comparisons with other eukaryotic MAP3Ks were also conducted to confirm protein identification (data not shown). Full-length PKs were aligned with ClustalW (see Supplemental Data Set 6 online) using plant MAP3K At-MEKK1 as an outgroup. The following alignment parameters were used: for pairwise alignment, gap opening, 10.0, and gap extension, 0.1; for multiple alignment, gap opening, 10.0, and gap extension, 0.20. Resulting alignments were submitted to MEGA4 software to generate a neighbor-joining tree derived from 5000 replicates. Bootstrap values are indicated on the nodes of each branch. A colored circle depicts each type of MAP3K and a species acronym indicates the origin of each protein (Table 1; see Supplemental Data Set 3 online). In relevant cases, previous MAP3K nomenclature is indicated in parentheses.
Figure 5.
Figure 5.
Mating, Filamentous Growth, and Virulence in U. maydis. In Ustilago, several MAPKs regulate mating by acting downstream of the pheromone receptor (see text for details). Along with cAMP signaling, MAPKs are also involved in filamentous growth and virulence. The cAMP pathway comprises heterotrimeric G proteins that function upstream of the adenylate cyclase Uac1. cAMP-dependent PKA holoenzyme works as a tetramer comprising two catalytic subunits (Adr1) and two regulatory subunits (Ubc1). When cAMP level is low, binding of regulatory subunits prevents catalytic activity. At higher cAMP levels, conformational changes allow release of catalytic subunits that enter in the nucleus. MAPK and cAMP signaling converge toward TF Prf1, which controls expression of pheromone- and virulence-induced genes. Hap2 is another MAPK substrate controlling expression of Prf1. In light of this study, previous MAPK names are depicted in parentheses. This figure has been adapted from Nadal et al. (2008).
Figure 6.
Figure 6.
The Pathogenicity Pathway from M. oryzae. Following sensing of host signals, the pathogenicity pathway is activated. Components mediating early steps of signal transduction converge toward a protein complex comprising Mst50 and MAPK signaling components. Following activation by Ste7, the Kss1 MAPK stimulates differentiation of appressoria and controls formation of turgor pressure. Nuclear localization of Kss1 is consistent with the fact that TFs accomplish MAPK function. Study of Mst12 indicates that IRM and infectious growth are separated processes, both required for full pathogenicity. Mst12 is not involved in appressorium formation but functions downstream of Kss1 to control penetration peg formation and proliferation inside host tissues. Sfl1 is another MAPK substrate regulating expression of stress-related genes. In light of this study, previous MAPK names are depicted in parentheses. This figure has been adapted from Park et al. (2006). AP, appressorium; CO, conidia; CU, cuticule; IH, infection hyphae; N, nucleus; PC, plant cell; PP, penetration peg.
Figure 7.
Figure 7.
MAPK Signaling during Interaction of Pathogenic Fungi and Plants. Fungal pathogens perceive plant-derived signals using plasma membrane receptors. This leads to the activation of fungal MAPK cascades that modulate TF activity and promote expression of genetic targets. Among induced genes are those associated with mating, IRM, mycotoxin biosynthesis, and degradation of the plant cell wall. On the other hand, plant receptors perceive molecular signatures associated with fungal structures or activity. This results in the activation of plant signaling pathways, including modified Ca2+ homeostasis, oxidative burst, and changes in MAPK phosphorylation status. Plant MAPKs promote biosynthesis of stress hormone and modulate gene expression through the phosphorylation of TFs. Output responses, including cell wall–degrading enzymes and antimicrobial compounds, affect fungal cell integrity and threaten pathogen survival. Fungal MAPK cascades also participate in compensatory responses allowing protection of hyphae against plant defenses. Overall, MAPK cascades can be viewed as conserved signaling modules involved in the molecular dialogue between fungal pathogens and plants. AP, appressorium; CO, conidia; CU, cuticule; CW, cell wall; CY, cytoplasm; GT, germ tube; N, nucleus; NM, nuclear membrane; PM, plasma membrane; PP, penetration peg; ROS, reactive oxygen species.
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References

    1. Ahn I.P., Suh S.C. (2007). Calcium/calmodulin-dependent signaling for pre-penetration development in Cochliobolus miyabeanus infecting rice. J. Gen. Plant Pathol. 73: 113–120
    1. Amselem J., et al. (2011). Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 7: e1002230. - PMC - PubMed
    1. Andreasson E., Ellis B. (2010). Convergence and specificity in the Arabidopsis MAPK nexus. Trends Plant Sci. 15: 106–113 - PubMed
    1. Andreasson E., et al. (2005). The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J. 24: 2579–2589 - PMC - PubMed
    1. Andrews D.L., Egan J.D., Mayorga M.E., Gold S.E. (2000). The Ustilago maydis ubc4 and ubc5 genes encode members of a MAP kinase cascade required for filamentous growth. Mol. Plant Microbe Interact. 13: 781–786 - PubMed

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