Functional Analysis of Two Affinity cAMP Phosphodiesterases in the Nematode-Trapping Fungus <i>Arthrobotrys oligospora</i>

Phosphodiesterases are essential regulators of cyclic nucleotide signaling with diverse physiological functions. Two phosphodiesterases, PdeH and PdeL, have been identified from yeast and filamentous fungi. Here, the orthologs of PdeH and PdeL were characterized in a typical nematode-trapping fungus...

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Main Authors: Ni Ma, Ke-Xin Jiang, Na Bai, Dong-Ni Li, Ke-Qin Zhang, Jin-Kui Yang
Format: Article
Language:English
Published: MDPI AG 2022-03-01
Series:Pathogens
Subjects:
Online Access:https://www.mdpi.com/2076-0817/11/4/405
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author Ni Ma
Ke-Xin Jiang
Na Bai
Dong-Ni Li
Ke-Qin Zhang
Jin-Kui Yang
author_facet Ni Ma
Ke-Xin Jiang
Na Bai
Dong-Ni Li
Ke-Qin Zhang
Jin-Kui Yang
author_sort Ni Ma
collection DOAJ
description Phosphodiesterases are essential regulators of cyclic nucleotide signaling with diverse physiological functions. Two phosphodiesterases, PdeH and PdeL, have been identified from yeast and filamentous fungi. Here, the orthologs of PdeH and PdeL were characterized in a typical nematode-trapping fungus <i>Arthrobotrys oligospora</i> by gene disruption and phenotypic comparison. Deletion of <i>AopdeH</i> caused serious defects in mycelial growth, conidiation, stress response, trap formation, and nematicidal efficiency compared to the wild-type strain. In contrast, these phenotypes have no significant difference in the absence of <i>AopdeL</i>. In addition, deletion of <i>AopdeH</i> and <i>AopdeL</i> resulted in a remarkable increase in cAMP level during vegetative growth and trap formation, and the number of autophagosomes was decreased in Δ<i>AopdeH</i> and Δ<i>AopdeL</i> mutants, whereas their volumes considerably increased. Moreover, metabolomic analyses revealed that many metabolites were downregulated in Δ<i>AopdeH</i> mutant compared to their expression in the wild-type strain. Our results indicate that AoPdeH plays a crucial role in mycelial growth, conidiation, stress response, secondary metabolism, and trap formation. In contrast, AoPdeL only plays a minor role in hyphal and conidial morphology, autophagy, and trap formation in <i>A. oligospora</i>. This work expands the roles of phosphodiesterases and deepens the understanding of the regulation of trap formation in nematode-trapping fungi.
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spelling doaj.art-32dd2e2e657441a8b90db8797b713cb32023-12-03T13:48:49ZengMDPI AGPathogens2076-08172022-03-0111440510.3390/pathogens11040405Functional Analysis of Two Affinity cAMP Phosphodiesterases in the Nematode-Trapping Fungus <i>Arthrobotrys oligospora</i>Ni Ma0Ke-Xin Jiang1Na Bai2Dong-Ni Li3Ke-Qin Zhang4Jin-Kui Yang5State Key Laboratory for Conservation and Utilization of Bio-Resources, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan University, Kunming 650091, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan University, Kunming 650091, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan University, Kunming 650091, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan University, Kunming 650091, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan University, Kunming 650091, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan University, Kunming 650091, ChinaPhosphodiesterases are essential regulators of cyclic nucleotide signaling with diverse physiological functions. Two phosphodiesterases, PdeH and PdeL, have been identified from yeast and filamentous fungi. Here, the orthologs of PdeH and PdeL were characterized in a typical nematode-trapping fungus <i>Arthrobotrys oligospora</i> by gene disruption and phenotypic comparison. Deletion of <i>AopdeH</i> caused serious defects in mycelial growth, conidiation, stress response, trap formation, and nematicidal efficiency compared to the wild-type strain. In contrast, these phenotypes have no significant difference in the absence of <i>AopdeL</i>. In addition, deletion of <i>AopdeH</i> and <i>AopdeL</i> resulted in a remarkable increase in cAMP level during vegetative growth and trap formation, and the number of autophagosomes was decreased in Δ<i>AopdeH</i> and Δ<i>AopdeL</i> mutants, whereas their volumes considerably increased. Moreover, metabolomic analyses revealed that many metabolites were downregulated in Δ<i>AopdeH</i> mutant compared to their expression in the wild-type strain. Our results indicate that AoPdeH plays a crucial role in mycelial growth, conidiation, stress response, secondary metabolism, and trap formation. In contrast, AoPdeL only plays a minor role in hyphal and conidial morphology, autophagy, and trap formation in <i>A. oligospora</i>. This work expands the roles of phosphodiesterases and deepens the understanding of the regulation of trap formation in nematode-trapping fungi.https://www.mdpi.com/2076-0817/11/4/405<i>Arthrobotrys oligospora</i>phosphodiesteraseconidiationstress responsetrap formationsecondary metabolism
spellingShingle Ni Ma
Ke-Xin Jiang
Na Bai
Dong-Ni Li
Ke-Qin Zhang
Jin-Kui Yang
Functional Analysis of Two Affinity cAMP Phosphodiesterases in the Nematode-Trapping Fungus <i>Arthrobotrys oligospora</i>
Pathogens
<i>Arthrobotrys oligospora</i>
phosphodiesterase
conidiation
stress response
trap formation
secondary metabolism
title Functional Analysis of Two Affinity cAMP Phosphodiesterases in the Nematode-Trapping Fungus <i>Arthrobotrys oligospora</i>
title_full Functional Analysis of Two Affinity cAMP Phosphodiesterases in the Nematode-Trapping Fungus <i>Arthrobotrys oligospora</i>
title_fullStr Functional Analysis of Two Affinity cAMP Phosphodiesterases in the Nematode-Trapping Fungus <i>Arthrobotrys oligospora</i>
title_full_unstemmed Functional Analysis of Two Affinity cAMP Phosphodiesterases in the Nematode-Trapping Fungus <i>Arthrobotrys oligospora</i>
title_short Functional Analysis of Two Affinity cAMP Phosphodiesterases in the Nematode-Trapping Fungus <i>Arthrobotrys oligospora</i>
title_sort functional analysis of two affinity camp phosphodiesterases in the nematode trapping fungus i arthrobotrys oligospora i
topic <i>Arthrobotrys oligospora</i>
phosphodiesterase
conidiation
stress response
trap formation
secondary metabolism
url https://www.mdpi.com/2076-0817/11/4/405
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