Two Phosphodiesterase Genes, PDEL and PDEH, Regulate Development and Pathogenicity by Modulating Intracellular Cyclic AMP Levels in Magnaporthe oryzae

Haifeng Zhang,Xiaobo Zheng,Wei Tang,Kaiyue Liu,Ping Wang,Qian Zhao,Jiansheng Wang,Min Guo,Zhengguang Zhang,Xing Zhang,Chaoyang Xue

doi:10.1371/journal.pone.0017241

Haifeng Zhang, Xiaobo Zheng + Show 9 more

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https://doi.org/10.1371/journal.pone.0017241

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Journal: PloS one	Publication Date: Feb 28, 2011
Citations: 159	License type: CC BY 4.0

Affiliation: Nanjing Agricultural University

Abstract

Cyclic AMP (cAMP) signaling plays an important role in regulating multiple cellular responses, such as growth, morphogenesis, and/or pathogenicity of eukaryotic organisms such as fungi. As a second messenger, cAMP is important in the activation of downstream effector molecules. The balance of intracellular cAMP levels depends on biosynthesis by adenylyl cyclases (ACs) and hydrolysis by cAMP phosphodiesterases (PDEases). The rice blast fungus Magnaporthe oryzae contains a high-affinity (PdeH/Pde2) and a low-affinity (PdeL/Pde1) PDEases, and a previous study showed that PdeH has a major role in asexual differentiation and pathogenicity. Here, we show that PdeL is required for asexual development and conidial morphology, and it also plays a minor role in regulating cAMP signaling. This is in contrast to PdeH whose mutation resulted in major defects in conidial morphology, cell wall integrity, and surface hydrophobicity, as well as a significant reduction in pathogenicity. Consistent with both PdeH and PdeL functioning in cAMP signaling, disruption of PDEH only partially rescued the mutant phenotype of ΔmagB and Δpka1. Further studies suggest that PdeH might function through a feedback mechanism to regulate the expression of pathogenicity factor Mpg1 during surface hydrophobicity and pathogenic development. Moreover, microarray data revealed new insights into the underlying cAMP regulatory mechanisms that may help to identify potential pathogenicity factors for the development of new disease management strategies.

Highlights

Heterotrimeric G protein signaling is one of the most important mechanisms by which eukaryotic cells sense extracellular signals and integrate them into intrinsic signal transduction pathways, such as Cyclic AMP (cAMP)-dependent signaling pathway. cAMP is a ubiquitous second messenger produced in cells in response to hormones and nutrients [1]
Cyclic AMP signaling plays an important role in regulating the growth and differentiation of eukaryotic organisms, including rice blast pathogen M. oryzae
We found that deletion of PDEH resulted in defects in conidial morphology, cell wall integrity, and surface hydrophobicity, as well as a significant reduction in pathogenicity

Summary

Introduction

Heterotrimeric G protein signaling is one of the most important mechanisms by which eukaryotic cells sense extracellular signals and integrate them into intrinsic signal transduction pathways, such as cAMP-dependent signaling pathway. cAMP is a ubiquitous second messenger produced in cells in response to hormones and nutrients [1]. CAMP plays an important role in activating downstream signaling components, such as phosphorylating enzyme protein kinase A (PKA). Both cAMP and PKA play key roles in the phosphorylation and regulation of enzyme substrates involved in intermediary metabolism [1]. In Saccharomyces cerevisiae, intracellular cAMP levels are regulated by the activity of the low- and high-affinity PDEases, Pde and Pde, respectively. Pde is a high-affinity PDEase expressed in many organisms ranging from fungi to mammals [2]. The low-affinity PDEase Pde is less well characterized but has been found in a wide range of organisms, including S. cerevisiae, Schizosaccharomyces pombe, Candida albicans, Dictyostelium discoideum, Vibrio fischeri, Leishmania mexicana, Trypanosoma brucei, and Trypanosoma cruzi [3,4,5,6,7,8,9,10]

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