GmMKK4‐activated GmMPK6 stimulates GmERF113 to trigger resistance to Phytophthora sojae in soybean

SUMMARY Phytophthora root and stem rot is a worldwide soybean (Glycine max) disease caused by the soil‐borne pathogen Phytophthora sojae. This disease is devastating to soybean production, so improvement of resistance to P. sojae is a major target in soybean breeding. Mitogen‐activated protein kinas...

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Veröffentlicht in:The Plant journal : for cell and molecular biology 2022-07, Vol.111 (2), p.473-495
Hauptverfasser: Gao, Hong, Jiang, Liangyu, Du, Banghan, Ning, Bin, Ding, Xiaodong, Zhang, Chuanzhong, Song, Bo, Liu, Shanshan, Zhao, Ming, Zhao, Yuxin, Rong, Tianyu, Liu, Dongxue, Wu, Junjiang, Xu, Pengfei, Zhang, Shuzhen
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container_issue 2
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container_title The Plant journal : for cell and molecular biology
container_volume 111
creator Gao, Hong
Jiang, Liangyu
Du, Banghan
Ning, Bin
Ding, Xiaodong
Zhang, Chuanzhong
Song, Bo
Liu, Shanshan
Zhao, Ming
Zhao, Yuxin
Rong, Tianyu
Liu, Dongxue
Wu, Junjiang
Xu, Pengfei
Zhang, Shuzhen
description SUMMARY Phytophthora root and stem rot is a worldwide soybean (Glycine max) disease caused by the soil‐borne pathogen Phytophthora sojae. This disease is devastating to soybean production, so improvement of resistance to P. sojae is a major target in soybean breeding. Mitogen‐activated protein kinase (MAPK) cascades are important signaling modules that convert environmental stimuli into cellular responses. Compared with extensive studies in Arabidopsis, the molecular mechanism of MAPK cascades in soybean disease resistance is barely elucidated. In this work, we found that the gene expression of mitogen‐activated protein kinase 6 (GmMPK6) was potently induced by P. sojae infection in the disease‐resistant soybean cultivar ‘Suinong 10’. Overexpression of GmMPK6 in soybean resulted in enhanced resistance to P. sojae and silencing of GmMPK6 led to the opposite phenotype. In our attempt to dissect the role of GmMPK6 in soybean resistance to phytophthora disease, we found that MAPK kinase 4 (GmMKK4) and the ERF transcription factor GmERF113 physically interact with GmMPK6, and we determined that GmMKK4 could phosphorylate and activate GmMPK6, which could subsequently phosphorylate GmERF113 upon P. sojae infection, suggesting that P. sojae can stimulate the GmMKK4–GmMPK6–GmERF113 signaling pathway in soybean. Moreover, phosphorylation of GmERF113 by the GmMKK4–GmMPK6 module promoted GmERF113 stability, nuclear localization and transcriptional activity, which significantly enhanced expression of the defense‐related genes GmPR1 and GmPR10‐1 and hence improved disease resistance of the transgenic soybean seedlings. In all, our data reveal that the GmMKK4–GmMPK6–GmERF113 cascade triggers resistance to P. sojae in soybean and shed light on functions of MAPK kinases in plant disease resistance. Significance Statement The GmMKK4–GmMPK6–GmERF113 cascade enhances resistance to soybean (Glycine max) phytophthora disease by successive phosphorylation events triggered by Phytophthora sojae. Our work provides new perspectives to develop strategies to improve plant disease resistance and insights into the roles of MAPK cascades in resistance against root and stem rot diseases.
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This disease is devastating to soybean production, so improvement of resistance to P. sojae is a major target in soybean breeding. Mitogen‐activated protein kinase (MAPK) cascades are important signaling modules that convert environmental stimuli into cellular responses. Compared with extensive studies in Arabidopsis, the molecular mechanism of MAPK cascades in soybean disease resistance is barely elucidated. In this work, we found that the gene expression of mitogen‐activated protein kinase 6 (GmMPK6) was potently induced by P. sojae infection in the disease‐resistant soybean cultivar ‘Suinong 10’. Overexpression of GmMPK6 in soybean resulted in enhanced resistance to P. sojae and silencing of GmMPK6 led to the opposite phenotype. In our attempt to dissect the role of GmMPK6 in soybean resistance to phytophthora disease, we found that MAPK kinase 4 (GmMKK4) and the ERF transcription factor GmERF113 physically interact with GmMPK6, and we determined that GmMKK4 could phosphorylate and activate GmMPK6, which could subsequently phosphorylate GmERF113 upon P. sojae infection, suggesting that P. sojae can stimulate the GmMKK4–GmMPK6–GmERF113 signaling pathway in soybean. Moreover, phosphorylation of GmERF113 by the GmMKK4–GmMPK6 module promoted GmERF113 stability, nuclear localization and transcriptional activity, which significantly enhanced expression of the defense‐related genes GmPR1 and GmPR10‐1 and hence improved disease resistance of the transgenic soybean seedlings. In all, our data reveal that the GmMKK4–GmMPK6–GmERF113 cascade triggers resistance to P. sojae in soybean and shed light on functions of MAPK kinases in plant disease resistance. Significance Statement The GmMKK4–GmMPK6–GmERF113 cascade enhances resistance to soybean (Glycine max) phytophthora disease by successive phosphorylation events triggered by Phytophthora sojae. 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This disease is devastating to soybean production, so improvement of resistance to P. sojae is a major target in soybean breeding. Mitogen‐activated protein kinase (MAPK) cascades are important signaling modules that convert environmental stimuli into cellular responses. Compared with extensive studies in Arabidopsis, the molecular mechanism of MAPK cascades in soybean disease resistance is barely elucidated. In this work, we found that the gene expression of mitogen‐activated protein kinase 6 (GmMPK6) was potently induced by P. sojae infection in the disease‐resistant soybean cultivar ‘Suinong 10’. Overexpression of GmMPK6 in soybean resulted in enhanced resistance to P. sojae and silencing of GmMPK6 led to the opposite phenotype. In our attempt to dissect the role of GmMPK6 in soybean resistance to phytophthora disease, we found that MAPK kinase 4 (GmMKK4) and the ERF transcription factor GmERF113 physically interact with GmMPK6, and we determined that GmMKK4 could phosphorylate and activate GmMPK6, which could subsequently phosphorylate GmERF113 upon P. sojae infection, suggesting that P. sojae can stimulate the GmMKK4–GmMPK6–GmERF113 signaling pathway in soybean. Moreover, phosphorylation of GmERF113 by the GmMKK4–GmMPK6 module promoted GmERF113 stability, nuclear localization and transcriptional activity, which significantly enhanced expression of the defense‐related genes GmPR1 and GmPR10‐1 and hence improved disease resistance of the transgenic soybean seedlings. In all, our data reveal that the GmMKK4–GmMPK6–GmERF113 cascade triggers resistance to P. sojae in soybean and shed light on functions of MAPK kinases in plant disease resistance. Significance Statement The GmMKK4–GmMPK6–GmERF113 cascade enhances resistance to soybean (Glycine max) phytophthora disease by successive phosphorylation events triggered by Phytophthora sojae. 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This disease is devastating to soybean production, so improvement of resistance to P. sojae is a major target in soybean breeding. Mitogen‐activated protein kinase (MAPK) cascades are important signaling modules that convert environmental stimuli into cellular responses. Compared with extensive studies in Arabidopsis, the molecular mechanism of MAPK cascades in soybean disease resistance is barely elucidated. In this work, we found that the gene expression of mitogen‐activated protein kinase 6 (GmMPK6) was potently induced by P. sojae infection in the disease‐resistant soybean cultivar ‘Suinong 10’. Overexpression of GmMPK6 in soybean resulted in enhanced resistance to P. sojae and silencing of GmMPK6 led to the opposite phenotype. In our attempt to dissect the role of GmMPK6 in soybean resistance to phytophthora disease, we found that MAPK kinase 4 (GmMKK4) and the ERF transcription factor GmERF113 physically interact with GmMPK6, and we determined that GmMKK4 could phosphorylate and activate GmMPK6, which could subsequently phosphorylate GmERF113 upon P. sojae infection, suggesting that P. sojae can stimulate the GmMKK4–GmMPK6–GmERF113 signaling pathway in soybean. Moreover, phosphorylation of GmERF113 by the GmMKK4–GmMPK6 module promoted GmERF113 stability, nuclear localization and transcriptional activity, which significantly enhanced expression of the defense‐related genes GmPR1 and GmPR10‐1 and hence improved disease resistance of the transgenic soybean seedlings. In all, our data reveal that the GmMKK4–GmMPK6–GmERF113 cascade triggers resistance to P. sojae in soybean and shed light on functions of MAPK kinases in plant disease resistance. Significance Statement The GmMKK4–GmMPK6–GmERF113 cascade enhances resistance to soybean (Glycine max) phytophthora disease by successive phosphorylation events triggered by Phytophthora sojae. Our work provides new perspectives to develop strategies to improve plant disease resistance and insights into the roles of MAPK cascades in resistance against root and stem rot diseases.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>35562858</pmid><doi>10.1111/tpj.15809</doi><tpages>495</tpages><orcidid>https://orcid.org/0000-0003-3554-5855</orcidid><orcidid>https://orcid.org/0000-0002-3311-0092</orcidid></addata></record>
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subjects Arabidopsis - metabolism
Crop production
Cultivars
Disease resistance
Disease Resistance - genetics
Environmental effects
Ethylene response factor (ERF) transcription factor
Gene expression
Glycine max
Glycine max - metabolism
Kinases
Localization
MAP kinase
Mitogen‐activated protein kinase cascade (MAPK)
Modules
Phenotypes
Phosphorylation
Phytophthora - physiology
Phytophthora sojae
Plant Breeding
Plant diseases
Plant immunity
Plant Proteins - metabolism
Protein kinase
Proteins
Seedlings
Signal transduction
Signaling
soybean
Soybeans
Stem rot
title GmMKK4‐activated GmMPK6 stimulates GmERF113 to trigger resistance to Phytophthora sojae in soybean
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