Abstract
In Magnaporthe oryzae, the causal ascomycete of the devastating rice blast disease, the conidial germ tube tip must sense and respond to a wide array of requisite cues from the host in order to switch from polarized to isotropic growth, ultimately forming the dome-shaped infection cell known as the appressorium. Although the role for G-protein mediated Cyclic AMP signaling in appressorium formation was first identified almost two decades ago, little is known about the spatio-temporal dynamics of the cascade and how the signal is transmitted through the intracellular network during cell growth and morphogenesis. In this study, we demonstrate that the late endosomal compartments, comprising of a PI3P-rich (Phosphatidylinositol 3-phosphate) highly dynamic tubulo-vesicular network, scaffold active MagA/GαS, Rgs1 (a GAP for MagA), Adenylate cyclase and Pth11 (a non-canonical GPCR) in the likely absence of AKAP-like anchors during early pathogenic development in M. oryzae. Loss of HOPS component Vps39 and consequently the late endosomal function caused a disruption of adenylate cyclase localization, cAMP signaling and appressorium formation. Remarkably, exogenous cAMP rescued the appressorium formation defects associated with VPS39 deletion in M. oryzae. We propose that sequestration of key G-protein signaling components on dynamic late endosomes and/or endolysosomes, provides an effective molecular means to compartmentalize and control the spatio-temporal activation and rapid downregulation (likely via vacuolar degradation) of cAMP signaling amidst changing cellular geometry during pathogenic development in M. oryzae.
Highlights
Eukaryotes, ranging from yeasts to multicellular metazoans, interact with their environment, constantly sampling it for physicochemical signals or cues for proper growth and development
We demonstrate that the late endosomal compartment is a highly dynamic tubulo-vesicular network that apart from membrane trafficking anchors active Gprotein signaling components in M. oryzae and regulates the biogenesis and spatio-temporal dynamics of Cyclic AMP (cAMP) signaling
Utilizing specific mutant strains compromised for late endosomal function we demonstrate the importance of signal anchoring by late endosomes during the establishment and spread of blast disease in rice and barley
Summary
Eukaryotes, ranging from yeasts to multicellular metazoans, interact with their environment, constantly sampling it for physicochemical signals or cues for proper growth and development. Ligand activated receptors promote the exchange of GDP to GTP on cognate GaS subunit, triggering its dissociation from the bc, thereby rendering it active to signal downstream [1]. Both GaS?GTP and Gbc moieties subsequently propagate the signal through a host of downstream effectors, which include ion channels, adenylate cyclases, phosphodiesterases and phospholipases [2,3]. The foremost of these is adenylate cyclase that synthesizes the second messenger Cyclic AMP (cAMP) from ATP. Active signaling by the GaS?GTP persists until the bound GTP is hydrolyzed to GDP, by the intrinsic GTPase activity of GaS, permitting GaS to re-associate with Gbc to form an inactive complex, and thereby commencing a fresh cycle of signaling [1,4]
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