Contribution of the Mitochondrial Carbonic Anhydrase (MoCA1) to Conidiogenesis and Pathogenesis in Magnaporthe oryzae

The interconversion of CO2 and HCO3− catalyzed by carbonic anhydrases (CAs) is a fundamental biochemical process in organisms. During mammalian–pathogen interaction, both host and pathogen CAs play vital roles in resistance and pathogenesis; during planta–pathogen interaction, however, plant CAs fun...

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Main Authors: Yuejia Dang, Yi Wei, Wajjiha Batool, Xicen Sun, Xiaoqian Li, Shi-Hong Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.845570/full
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author Yuejia Dang
Yuejia Dang
Yi Wei
Yi Wei
Wajjiha Batool
Wajjiha Batool
Xicen Sun
Xicen Sun
Xiaoqian Li
Xiaoqian Li
Shi-Hong Zhang
Shi-Hong Zhang
author_facet Yuejia Dang
Yuejia Dang
Yi Wei
Yi Wei
Wajjiha Batool
Wajjiha Batool
Xicen Sun
Xicen Sun
Xiaoqian Li
Xiaoqian Li
Shi-Hong Zhang
Shi-Hong Zhang
author_sort Yuejia Dang
collection DOAJ
description The interconversion of CO2 and HCO3− catalyzed by carbonic anhydrases (CAs) is a fundamental biochemical process in organisms. During mammalian–pathogen interaction, both host and pathogen CAs play vital roles in resistance and pathogenesis; during planta–pathogen interaction, however, plant CAs function in host resistance but whether pathogen CAs are involved in pathogenesis is unknown. Here, we biologically characterized the Magnaporthe oryzae CA (MoCA1). Through detecting the DsRED-tagged proteins, we observed the fusion MoCA1 in the mitochondria of M. oryzae. Together with the measurement of CA activity, we confirmed that MoCA1 is a mitochondrial zinc-binding CA. MoCA1 expression, upregulated with H2O2 or NaHCO3 treatment, also showed a drastic upregulation during conidiogenesis and pathogenesis. When MoCA1 was deleted, the mutant ΔMoCA1 was defective in conidiophore development and pathogenicity. 3,3′-Diaminobenzidine (DAB) staining indicated that more H2O2 accumulated in ΔMoCA1; accordingly, ATPase genes were downregulated and ATP content decreased in ΔMoCA1. Summarily, our data proved the involvement of the mitochondrial MoCA1 in conidiogenesis and pathogenesis in the rice blast fungus. Considering the previously reported HCO3− transporter MoAE4, we propose that MoCA1 in cooperation with MoAE4 constitutes a HCO3− homeostasis-mediated disease pathway, in which MoCA1 and MoAE4 can be a drug target for disease control.
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spelling doaj.art-2eacaf8d53f14180b3e7eabe0426749c2022-12-21T23:59:55ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-02-011310.3389/fmicb.2022.845570845570Contribution of the Mitochondrial Carbonic Anhydrase (MoCA1) to Conidiogenesis and Pathogenesis in Magnaporthe oryzaeYuejia Dang0Yuejia Dang1Yi Wei2Yi Wei3Wajjiha Batool4Wajjiha Batool5Xicen Sun6Xicen Sun7Xiaoqian Li8Xiaoqian Li9Shi-Hong Zhang10Shi-Hong Zhang11Center for Extreme-Environmental Microorganisms, Shenyang Agricultural University, Shenyang, ChinaCollege of Plant Protection, Shenyang Agricultural University, Shenyang, ChinaCenter for Extreme-Environmental Microorganisms, Shenyang Agricultural University, Shenyang, ChinaCollege of Plant Protection, Shenyang Agricultural University, Shenyang, ChinaCenter for Extreme-Environmental Microorganisms, Shenyang Agricultural University, Shenyang, ChinaCollege of Plant Protection, Shenyang Agricultural University, Shenyang, ChinaCenter for Extreme-Environmental Microorganisms, Shenyang Agricultural University, Shenyang, ChinaCollege of Plant Protection, Shenyang Agricultural University, Shenyang, ChinaCenter for Extreme-Environmental Microorganisms, Shenyang Agricultural University, Shenyang, ChinaCollege of Plant Protection, Shenyang Agricultural University, Shenyang, ChinaCenter for Extreme-Environmental Microorganisms, Shenyang Agricultural University, Shenyang, ChinaCollege of Plant Protection, Shenyang Agricultural University, Shenyang, ChinaThe interconversion of CO2 and HCO3− catalyzed by carbonic anhydrases (CAs) is a fundamental biochemical process in organisms. During mammalian–pathogen interaction, both host and pathogen CAs play vital roles in resistance and pathogenesis; during planta–pathogen interaction, however, plant CAs function in host resistance but whether pathogen CAs are involved in pathogenesis is unknown. Here, we biologically characterized the Magnaporthe oryzae CA (MoCA1). Through detecting the DsRED-tagged proteins, we observed the fusion MoCA1 in the mitochondria of M. oryzae. Together with the measurement of CA activity, we confirmed that MoCA1 is a mitochondrial zinc-binding CA. MoCA1 expression, upregulated with H2O2 or NaHCO3 treatment, also showed a drastic upregulation during conidiogenesis and pathogenesis. When MoCA1 was deleted, the mutant ΔMoCA1 was defective in conidiophore development and pathogenicity. 3,3′-Diaminobenzidine (DAB) staining indicated that more H2O2 accumulated in ΔMoCA1; accordingly, ATPase genes were downregulated and ATP content decreased in ΔMoCA1. Summarily, our data proved the involvement of the mitochondrial MoCA1 in conidiogenesis and pathogenesis in the rice blast fungus. Considering the previously reported HCO3− transporter MoAE4, we propose that MoCA1 in cooperation with MoAE4 constitutes a HCO3− homeostasis-mediated disease pathway, in which MoCA1 and MoAE4 can be a drug target for disease control.https://www.frontiersin.org/articles/10.3389/fmicb.2022.845570/fullcarbonic anhydrasemitochondrionconidiophorepathogenesisMagnaporthe oryzae
spellingShingle Yuejia Dang
Yuejia Dang
Yi Wei
Yi Wei
Wajjiha Batool
Wajjiha Batool
Xicen Sun
Xicen Sun
Xiaoqian Li
Xiaoqian Li
Shi-Hong Zhang
Shi-Hong Zhang
Contribution of the Mitochondrial Carbonic Anhydrase (MoCA1) to Conidiogenesis and Pathogenesis in Magnaporthe oryzae
Frontiers in Microbiology
carbonic anhydrase
mitochondrion
conidiophore
pathogenesis
Magnaporthe oryzae
title Contribution of the Mitochondrial Carbonic Anhydrase (MoCA1) to Conidiogenesis and Pathogenesis in Magnaporthe oryzae
title_full Contribution of the Mitochondrial Carbonic Anhydrase (MoCA1) to Conidiogenesis and Pathogenesis in Magnaporthe oryzae
title_fullStr Contribution of the Mitochondrial Carbonic Anhydrase (MoCA1) to Conidiogenesis and Pathogenesis in Magnaporthe oryzae
title_full_unstemmed Contribution of the Mitochondrial Carbonic Anhydrase (MoCA1) to Conidiogenesis and Pathogenesis in Magnaporthe oryzae
title_short Contribution of the Mitochondrial Carbonic Anhydrase (MoCA1) to Conidiogenesis and Pathogenesis in Magnaporthe oryzae
title_sort contribution of the mitochondrial carbonic anhydrase moca1 to conidiogenesis and pathogenesis in magnaporthe oryzae
topic carbonic anhydrase
mitochondrion
conidiophore
pathogenesis
Magnaporthe oryzae
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.845570/full
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