MoImd4 mediates crosstalk between MoPdeH-cAMP signalling and purine metabolism to govern growth and pathogenicity in Magnaporthe oryzae.

Lina Yang,Haifeng Zhang,Xiaobo Zheng,Xinyu Liu,Zhengguang Zhang,Ping Wang,Yuhan Xiao,Ziyi Yin,Xingjia Cai,Yanyan Ru

doi:10.1111/mpp.12770

Abstract

SummaryThe high‐affinity cyclic adenosine monophosphate (cAMP) phosphodiesterase MoPdeH is important not only for cAMP signalling and pathogenicity, but also for cell wall integrity (CWI) maintenance in the rice blast fungus Magnaporthe oryzae. To explore the underlying mechanism, we identified MoImd4 as an inosine‐5′‐monophosphate dehydrogenase (IMPDH) homologue that interacts with MoPdeH. Targeted deletion of MoIMD4 resulted in reduced de novo purine biosynthesis and growth, as well as attenuated pathogenicity, which were suppressed by exogenous xanthosine monophosphate (XMP). Treatment with mycophenolic acid (MPA), which specifically inhibits MoImd4 activity, resulted in reduced growth and virulence attenuation. Intriguingly, further analysis showed that MoImd4 promotes the phosphodiesterase activity of MoPdeH, thereby decreasing intracellular cAMP levels, and MoPdeH also promotes the IMPDH activity of MoImd4. Our studies revealed the presence of a novel crosstalk between cAMP regulation and purine biosynthesis in M. oryzae, and indicated that such a link is also important in the pathogenesis of M. oryzae.

Highlights

MoPdeH is a high-affinity phosphodiesterase that hydrolyses intracellular cyclic adenosine monophosphate (cAMP) required for the vegetative growth, functional appressorium development and virulence of M. oryzae (Ramanujam and Naqvi, 2010; Yang et al, 2017; Zhang et al, 2011aa)
MGG_03699 shares high amino acid sequence homology with inosine monophosphate dehydrogenases (Imds) from various species (Figs 1A, S2 and Table S1, see Supporting Information). To test whether this Imd homologue encodes conserved functions, we expressed the protein with the yeast expression vector pYES2 in ∆Scimd3 and ∆Scimd4 strains, and found that the M. oryzae protein could partially rescue the growth defect of ∆Scimd4 (Fig. 1D,E)
The results indicate that the hydrolytic activity of MoImd4 and xanthosine monophosphate (XMP) levels are critical for the pathogenicity of M. oryzae

Summary

Introduction

In the rice blast fungus Magnaporthe oryzae, the cyclic adenosine monophosphate (cAMP) signalling pathway plays an important role in vegetative growth, asexual/sexual development, cell wall integrity (CWI), appressorium formation and virulence (Lee and Dean, 1993; Liu et al, 2016b; Ramanujam and Naqvi, 2010; Yang et al, 2017; Yin et al, 2016; Zhang et al, 2011a, 2011b). In M. oryzae, intracellular cAMP levels are governed by the dynamic balance between adenylyl cyclase MoMac, which synthesizes cAMP, and high-affinity phosphodiesterase MoPdeH and low-affinity MoPdeL, which hydrolyse cAMP (Ramanujam and Naqvi, 2010; Woobong Choi, 1997; Yang et al, 2017; Zhang et al, 2011aa).

Results

Discussion

Conclusion