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Two phosphodiesterase genes, PDEL and PDEH, regulate development and pathogenicity by modulating intracellular cyclic AMP levels in Magnaporthe oryzae.

Zhang H, Liu K, Zhang X, Tang W, Wang J, Guo M, Zhao Q, Zheng X, Wang P, Zhang Z - PLoS ONE (2011)

Bottom Line: As a second messenger, cAMP is important in the activation of downstream effector molecules.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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Agriculture, Nanjing, China.

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.

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Related in: MedlinePlus

The loss of PDEH leads to reduced pathogenicity and induction of strong plant defense responses.(A) Spraying assay. Five milliliters of conidial suspension (5×104 spores/ml) of each strain were sprayed on rice seedlings. Diseased leaves were photographed 7 days after inoculation. (B) Detached leaf assay. The hyphal plugs of each strain were placed onto the upside of detached rice seedling leaves. Diseased leaves were photographed 5 days after inoculation. (C) Observation of infectious growth. Excised rice sheath from 4-week-old rice seedlings was inoculated with conidial suspension (5×104 spores/ml of each strain). Infectious growth was observed 48 hours after inoculation. (D) The expression of rice pathogenesis-related (PR) genes over time after inoculation. The transcriptional expression of PR1a and PBZ1 in the infected rice was analyzed using quantitative RT-PCR. The graph was generated with three replicates in a representative data set, and similar results were obtained in another independent biological repetition. The error bars indicate SD of three replicates.
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pone-0017241-g007: The loss of PDEH leads to reduced pathogenicity and induction of strong plant defense responses.(A) Spraying assay. Five milliliters of conidial suspension (5×104 spores/ml) of each strain were sprayed on rice seedlings. Diseased leaves were photographed 7 days after inoculation. (B) Detached leaf assay. The hyphal plugs of each strain were placed onto the upside of detached rice seedling leaves. Diseased leaves were photographed 5 days after inoculation. (C) Observation of infectious growth. Excised rice sheath from 4-week-old rice seedlings was inoculated with conidial suspension (5×104 spores/ml of each strain). Infectious growth was observed 48 hours after inoculation. (D) The expression of rice pathogenesis-related (PR) genes over time after inoculation. The transcriptional expression of PR1a and PBZ1 in the infected rice was analyzed using quantitative RT-PCR. The graph was generated with three replicates in a representative data set, and similar results were obtained in another independent biological repetition. The error bars indicate SD of three replicates.

Mentions: To determine whether PDEL and PDEH are involved in pathogenesis, conidial suspensions were sprayed onto susceptible rice seedlings and hyphal plugs were placed onto detached rice seedling leaves (CO-39 cv. oryzae) to develop rice blast lesions. In a spray-inoculation test, the ΔpdeH mutant produced tiny and restricted lesions, whereas the ΔpdeL mutant, wild-type, and complement strains showed susceptible-type spreading lesions (Figure 7A). In a detached-inoculation test, lesions caused by ΔpdeH mutant hyphal plugs spread very slowly and the lesion sizes were small, while those caused by ΔpdeL mutant, wild type, and complement strains spread rapidly and the neighboring lesions joined together by 5 days after inoculation (Figure 7B).


Two phosphodiesterase genes, PDEL and PDEH, regulate development and pathogenicity by modulating intracellular cyclic AMP levels in Magnaporthe oryzae.

Zhang H, Liu K, Zhang X, Tang W, Wang J, Guo M, Zhao Q, Zheng X, Wang P, Zhang Z - PLoS ONE (2011)

The loss of PDEH leads to reduced pathogenicity and induction of strong plant defense responses.(A) Spraying assay. Five milliliters of conidial suspension (5×104 spores/ml) of each strain were sprayed on rice seedlings. Diseased leaves were photographed 7 days after inoculation. (B) Detached leaf assay. The hyphal plugs of each strain were placed onto the upside of detached rice seedling leaves. Diseased leaves were photographed 5 days after inoculation. (C) Observation of infectious growth. Excised rice sheath from 4-week-old rice seedlings was inoculated with conidial suspension (5×104 spores/ml of each strain). Infectious growth was observed 48 hours after inoculation. (D) The expression of rice pathogenesis-related (PR) genes over time after inoculation. The transcriptional expression of PR1a and PBZ1 in the infected rice was analyzed using quantitative RT-PCR. The graph was generated with three replicates in a representative data set, and similar results were obtained in another independent biological repetition. The error bars indicate SD of three replicates.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3046207&req=5

pone-0017241-g007: The loss of PDEH leads to reduced pathogenicity and induction of strong plant defense responses.(A) Spraying assay. Five milliliters of conidial suspension (5×104 spores/ml) of each strain were sprayed on rice seedlings. Diseased leaves were photographed 7 days after inoculation. (B) Detached leaf assay. The hyphal plugs of each strain were placed onto the upside of detached rice seedling leaves. Diseased leaves were photographed 5 days after inoculation. (C) Observation of infectious growth. Excised rice sheath from 4-week-old rice seedlings was inoculated with conidial suspension (5×104 spores/ml of each strain). Infectious growth was observed 48 hours after inoculation. (D) The expression of rice pathogenesis-related (PR) genes over time after inoculation. The transcriptional expression of PR1a and PBZ1 in the infected rice was analyzed using quantitative RT-PCR. The graph was generated with three replicates in a representative data set, and similar results were obtained in another independent biological repetition. The error bars indicate SD of three replicates.
Mentions: To determine whether PDEL and PDEH are involved in pathogenesis, conidial suspensions were sprayed onto susceptible rice seedlings and hyphal plugs were placed onto detached rice seedling leaves (CO-39 cv. oryzae) to develop rice blast lesions. In a spray-inoculation test, the ΔpdeH mutant produced tiny and restricted lesions, whereas the ΔpdeL mutant, wild-type, and complement strains showed susceptible-type spreading lesions (Figure 7A). In a detached-inoculation test, lesions caused by ΔpdeH mutant hyphal plugs spread very slowly and the lesion sizes were small, while those caused by ΔpdeL mutant, wild type, and complement strains spread rapidly and the neighboring lesions joined together by 5 days after inoculation (Figure 7B).

Bottom Line: As a second messenger, cAMP is important in the activation of downstream effector molecules.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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Agriculture, Nanjing, China.

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.

Show MeSH
Related in: MedlinePlus