Multiple Plant Surface Signals are Sensed by Different Mechanisms in the Rice Blast Fungus for Appressorium Formation

Abstract

Surface recognition and penetration are among the most critical plant infection processes in foliar pathogens. In Magnaporthe oryzae, the Pmk1 MAP kinase regulates appressorium formation and penetration. Its orthologs also are known to be required for various plant infection processes in other phytopathogenic fungi. Although a number of upstream components of this important pathway have been characterized, the upstream sensors for surface signals have not been well characterized. Pmk1 is orthologous to Kss1 in yeast that functions downstream from Msb2 and Sho1 for filamentous growth. Because of the conserved nature of the Pmk1 and Kss1 pathways and reduced expression of MoMSB2 in the pmk1 mutant, in this study we functionally characterized the MoMSB2 and MoSHO1 genes. Whereas the Momsb2 mutant was significantly reduced in appressorium formation and virulence, the Mosho1 mutant was only slightly reduced. The Mosho1 Momsb2 double mutant rarely formed appressoria on artificial hydrophobic surfaces, had a reduced Pmk1 phosphorylation level, and was nonresponsive to cutin monomers. However, it still formed appressoria and caused rare, restricted lesions on rice leaves. On artificial hydrophilic surfaces, leaf surface waxes and primary alcohols-but not paraffin waxes and alkanes- stimulated appressorium formation in the Mosho1 Momsb2 mutant, but more efficiently in the Momsb2 mutant. Furthermore, expression of a dominant active MST7 allele partially suppressed the defects of the Momsb2 mutant. These results indicate that, besides surface hydrophobicity and cutin monomers, primary alcohols, a major component of epicuticular leaf waxes in grasses, are recognized by M. oryzae as signals for appressorium formation. Our data also suggest that MoMsb2 and MoSho1 may have overlapping functions in recognizing various surface signals for Pmk1 activation and appressorium formation. While MoMsb2 is critical for sensing surface hydrophobicity and cutin monomers, MoSho1 may play a more important role in recognizing rice leaf waxes.

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

“…Many questions regarding fungal MAPK signaling remain unanswered, and upcoming studies should, for instance, focus on the understanding of upstream mechanisms leading to MAPK activation. Recently, homologs of the yeast osmosensors Sho1 and Msb2 (Figure 1) have been shown to act upstream of pathogenesis-related MAPK cascades in U. maydis ( Figure 5; Lanver et al, 2010), M. oryzae (Figure 6; Liu et al, 2011), and F. oxysporum (Pérez-Nadales and Di Pietro, 2011). Along with the previously identified G protein-coupled receptor Pth11 from M. oryzae (Figure 6; DeZwaan et al, 1999;Kulkarni et al, 2003), these candidate receptors likely ensure MAPK cascade activation following recognition of specific ligands.…”

The AngFus3 Mitogen-Activated Protein Kinase Controls Hyphal Differentiation and Secondary Metabolism in Aspergillus niger

“…In the gray mold Botrytis cinerea, the homologous signaling module is essential for the differentiation of sclerotia and contributes to the control of microconidiation (17). In various plant-parasitic fungi, MAP kinases are pathogenicity factors and are involved in plant surface recognition and the differentiation of infection structures, such as appressoria (18)(19)(20)(21).…”

Regulatory network of genes associated with stimuli sensing, signal transduction and physiological transformation of appressorium inMagnaporthe oryzae

“…The detail mechanisms underlying specificity of Msb2-mediated cutin monomer and surface hydrophobicity sensing, as well as the exact role of Sho1 in leaf wax sensing, are still unknown. It was, however, suggested that these proteins might play overlapping role in sensing appressorium inducing signals (Liu et al 2011). Surprisingly, targeted gene deletion of M. oryzae MoMSB 2 and MoSHO 2 did not significantly alter the progression of appressorium differentiation on host surface (Liu et al 2011) From these observations, the likely existence of yet to be identified proteins in the rice blast fungus with an overlapping role in mediating appressorium morphogenesis was speculated.…”

“…It was, however, suggested that these proteins might play overlapping role in sensing appressorium inducing signals (Liu et al 2011). Surprisingly, targeted gene deletion of M. oryzae MoMSB 2 and MoSHO 2 did not significantly alter the progression of appressorium differentiation on host surface (Liu et al 2011) From these observations, the likely existence of yet to be identified proteins in the rice blast fungus with an overlapping role in mediating appressorium morphogenesis was speculated. This hypothesis was confirmed recently after the CFEM (conserved fungal-specific extracellular membrane spanning) domain of PTH11 like GPCR (G-protein coupled receptors) was identified and characterised in M. oryzae .…”

“…Cutinases facilitate spore adhesion in Colletotrichum graminicola (Pascholati et al 1993), Uromyces viciae-fabae (Deising et al 1992) and Blumeria graminis (Pascholati et al 1992), carbon acquisition in Venturia inequalis (Köller et al 1991) and also promote the virulence of M. oryzae (Skamnioti and Gurr 2007). Cutinase-mediated degradation of plant cuticle into cutin monomers elicits the cAMP/PKA and DAG/PKC signalling cascades and triggers appressorium formation in M. oryzae (Skamnioti and Gurr 2007; Liu et al 2011). The M. oryzae genome encodes 17 putative cutinases (Dean et al 2005) including Cutinase1 ( CUT 1) and Cutinase2 ( CUT 2) that have been previously characterised (Sweigard et al 1992; Skamnioti and Gurr 2007).…”