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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Frontiers Media S.A.
2022-02-01
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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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publishDate | 2022-02-01 |
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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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