Apoplastic and cytoplasmic location of harpin protein Hpa1Xoo plays different roles in H2O2 generation and pathogen resistance in Arabidopsis

Harpin proteins secreted by phytopathogenic bacteria have been shown to activate the plant defense pathway, which involves transduction of a hydrogen peroxide (H 2 O 2 ) signal generated in the apoplast. However, the way in which harpins are recognized in the pathway and what role the apoplastic H 2...

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Published in	Plant molecular biology Vol. 79; no. 4-5; pp. 375 - 391
Main Authors	Sang, Suling, Li, Xiaojie, Gao, Rong, You, Zhenzhen, Lü, Beibei, Liu, Peiqing, Ma, Qixiang, Dong, Hansong
Format	Journal Article
Language	English
Published	Dordrecht Springer Netherlands 01.07.2012
Subjects	Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis - microbiology Bacterial Outer Membrane Proteins - genetics Bacterial Outer Membrane Proteins - metabolism Biochemistry Biological Transport, Active Biomedical and Life Sciences Cell Membrane - metabolism Cytoplasm - metabolism Extracellular Space - metabolism Genes, Bacterial Hydrogen Peroxide - metabolism Life Sciences Plant Diseases - microbiology Plant Pathology Plant Sciences Plants, Genetically Modified Recombinant Proteins - genetics Recombinant Proteins - metabolism Xanthomonas - genetics Xanthomonas - metabolism Xanthomonas - pathogenicity H Hpa1 Plant defenses Harpin Cytoplasmic translocation O
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Abstract	Harpin proteins secreted by phytopathogenic bacteria have been shown to activate the plant defense pathway, which involves transduction of a hydrogen peroxide (H 2 O 2 ) signal generated in the apoplast. However, the way in which harpins are recognized in the pathway and what role the apoplastic H 2 O 2 plays in plant defenses are unclear. Here, we examine whether the cellular localization of Hpa1 Xoo , a harpin protein produced by the rice bacterial leaf blight pathogen, impacts H 2 O 2 production and pathogen resistance in Arabidopsis thaliana . Transformation with the hpa1 Xoo gene and hpa1 Xoo fused to an apoplastic localization signal ( shpa1 Xoo ) generated h pa1 Xoo - and sh pa1 Xoo - e xpressing t ransgenic A . t haliana (HETAt and SHETAt) plants, respectively. Hpa1 Xoo was associated with the apoplast in SHETAt plants but localized inside the cell in HETAt plants. In addition, Hpa1 Xoo localization accompanied H 2 O 2 accumulation in both the apoplast and cytoplasm of SHETAt plants but only in the cytoplasm of HETAt plants. Apoplastic H 2 O 2 production via nicotinamide adenine dinucleotide phosphate (NADPH) oxidase (NOX) located in the plasma membrane is a common feature of plant defenses. In SHETAt plants, H 2 O 2 was generated in apoplasts in a NOX-dependent manner but accumulated to a greater extent in the cytoplasm than in the apoplast. After being applied to the wild-type plant, Hpa1 Xoo localized to apoplasts and stimulated H 2 O 2 production as in SHETAt plants. In both plants, inhibiting apoplastic H 2 O 2 generation abrogated both cytoplasmic H 2 O 2 accumulation and plant resistance to bacterial pathogens. These results suggest the possibility that the apoplastic H 2 O 2 is subject to a cytoplasmic translocation for participation in the pathogen defense.
AbstractList	Harpin proteins secreted by phytopathogenic bacteria have been shown to activate the plant defense pathway, which involves transduction of a hydrogen peroxide (H 2 O 2 ) signal generated in the apoplast. However, the way in which harpins are recognized in the pathway and what role the apoplastic H 2 O 2 plays in plant defenses are unclear. Here, we examine whether the cellular localization of Hpa1 Xoo , a harpin protein produced by the rice bacterial leaf blight pathogen, impacts H 2 O 2 production and pathogen resistance in Arabidopsis thaliana . Transformation with the hpa1 Xoo gene and hpa1 Xoo fused to an apoplastic localization signal ( shpa1 Xoo ) generated h pa1 Xoo - and sh pa1 Xoo - e xpressing t ransgenic A . t haliana (HETAt and SHETAt) plants, respectively. Hpa1 Xoo was associated with the apoplast in SHETAt plants but localized inside the cell in HETAt plants. In addition, Hpa1 Xoo localization accompanied H 2 O 2 accumulation in both the apoplast and cytoplasm of SHETAt plants but only in the cytoplasm of HETAt plants. Apoplastic H 2 O 2 production via nicotinamide adenine dinucleotide phosphate (NADPH) oxidase (NOX) located in the plasma membrane is a common feature of plant defenses. In SHETAt plants, H 2 O 2 was generated in apoplasts in a NOX-dependent manner but accumulated to a greater extent in the cytoplasm than in the apoplast. After being applied to the wild-type plant, Hpa1 Xoo localized to apoplasts and stimulated H 2 O 2 production as in SHETAt plants. In both plants, inhibiting apoplastic H 2 O 2 generation abrogated both cytoplasmic H 2 O 2 accumulation and plant resistance to bacterial pathogens. These results suggest the possibility that the apoplastic H 2 O 2 is subject to a cytoplasmic translocation for participation in the pathogen defense. Harpin proteins secreted by phytopathogenic bacteria have been shown to activate the plant defense pathway, which involves transduction of a hydrogen peroxide (H(2)O(2)) signal generated in the apoplast. However, the way in which harpins are recognized in the pathway and what role the apoplastic H(2)O(2) plays in plant defenses are unclear. Here, we examine whether the cellular localization of Hpa1(Xoo), a harpin protein produced by the rice bacterial leaf blight pathogen, impacts H(2)O(2) production and pathogen resistance in Arabidopsis thaliana. Transformation with the hpa1 (Xoo) gene and hpa1 (Xoo) fused to an apoplastic localization signal (shpa1 (Xoo)) generated h pa1 (Xoo)- and sh pa1 (Xoo)-expressing transgenic A . t haliana (HETAt and SHETAt) plants, respectively. Hpa1(Xoo) was associated with the apoplast in SHETAt plants but localized inside the cell in HETAt plants. In addition, Hpa1(Xoo) localization accompanied H(2)O(2) accumulation in both the apoplast and cytoplasm of SHETAt plants but only in the cytoplasm of HETAt plants. Apoplastic H(2)O(2) production via nicotinamide adenine dinucleotide phosphate (NADPH) oxidase (NOX) located in the plasma membrane is a common feature of plant defenses. In SHETAt plants, H(2)O(2) was generated in apoplasts in a NOX-dependent manner but accumulated to a greater extent in the cytoplasm than in the apoplast. After being applied to the wild-type plant, Hpa1(Xoo) localized to apoplasts and stimulated H(2)O(2) production as in SHETAt plants. In both plants, inhibiting apoplastic H(2)O(2) generation abrogated both cytoplasmic H(2)O(2) accumulation and plant resistance to bacterial pathogens. These results suggest the possibility that the apoplastic H(2)O(2) is subject to a cytoplasmic translocation for participation in the pathogen defense. Harpin proteins secreted by phytopathogenic bacteria have been shown to activate the plant defense pathway, which involves transduction of a hydrogen peroxide (H(2)O(2)) signal generated in the apoplast. However, the way in which harpins are recognized in the pathway and what role the apoplastic H(2)O(2) plays in plant defenses are unclear. Here, we examine whether the cellular localization of Hpa1(Xoo), a harpin protein produced by the rice bacterial leaf blight pathogen, impacts H(2)O(2) production and pathogen resistance in Arabidopsis thaliana. Transformation with the hpa1 (Xoo) gene and hpa1 (Xoo) fused to an apoplastic localization signal (shpa1 (Xoo)) generated h pa1 (Xoo)- and sh pa1 (Xoo)-expressing transgenic A . t haliana (HETAt and SHETAt) plants, respectively. Hpa1(Xoo) was associated with the apoplast in SHETAt plants but localized inside the cell in HETAt plants. In addition, Hpa1(Xoo) localization accompanied H(2)O(2) accumulation in both the apoplast and cytoplasm of SHETAt plants but only in the cytoplasm of HETAt plants. Apoplastic H(2)O(2) production via nicotinamide adenine dinucleotide phosphate (NADPH) oxidase (NOX) located in the plasma membrane is a common feature of plant defenses. In SHETAt plants, H(2)O(2) was generated in apoplasts in a NOX-dependent manner but accumulated to a greater extent in the cytoplasm than in the apoplast. After being applied to the wild-type plant, Hpa1(Xoo) localized to apoplasts and stimulated H(2)O(2) production as in SHETAt plants. In both plants, inhibiting apoplastic H(2)O(2) generation abrogated both cytoplasmic H(2)O(2) accumulation and plant resistance to bacterial pathogens. These results suggest the possibility that the apoplastic H(2)O(2) is subject to a cytoplasmic translocation for participation in the pathogen defense.Harpin proteins secreted by phytopathogenic bacteria have been shown to activate the plant defense pathway, which involves transduction of a hydrogen peroxide (H(2)O(2)) signal generated in the apoplast. However, the way in which harpins are recognized in the pathway and what role the apoplastic H(2)O(2) plays in plant defenses are unclear. Here, we examine whether the cellular localization of Hpa1(Xoo), a harpin protein produced by the rice bacterial leaf blight pathogen, impacts H(2)O(2) production and pathogen resistance in Arabidopsis thaliana. Transformation with the hpa1 (Xoo) gene and hpa1 (Xoo) fused to an apoplastic localization signal (shpa1 (Xoo)) generated h pa1 (Xoo)- and sh pa1 (Xoo)-expressing transgenic A . t haliana (HETAt and SHETAt) plants, respectively. Hpa1(Xoo) was associated with the apoplast in SHETAt plants but localized inside the cell in HETAt plants. In addition, Hpa1(Xoo) localization accompanied H(2)O(2) accumulation in both the apoplast and cytoplasm of SHETAt plants but only in the cytoplasm of HETAt plants. Apoplastic H(2)O(2) production via nicotinamide adenine dinucleotide phosphate (NADPH) oxidase (NOX) located in the plasma membrane is a common feature of plant defenses. In SHETAt plants, H(2)O(2) was generated in apoplasts in a NOX-dependent manner but accumulated to a greater extent in the cytoplasm than in the apoplast. After being applied to the wild-type plant, Hpa1(Xoo) localized to apoplasts and stimulated H(2)O(2) production as in SHETAt plants. In both plants, inhibiting apoplastic H(2)O(2) generation abrogated both cytoplasmic H(2)O(2) accumulation and plant resistance to bacterial pathogens. These results suggest the possibility that the apoplastic H(2)O(2) is subject to a cytoplasmic translocation for participation in the pathogen defense.
Author	Gao, Rong Ma, Qixiang Lü, Beibei Liu, Peiqing You, Zhenzhen Sang, Suling Dong, Hansong Li, Xiaojie
Author_xml	– sequence: 1 givenname: Suling surname: Sang fullname: Sang, Suling organization: State Ministry of Education Key Laboratory of Integrated Management of Crop Pests, Nanjing Agricultural University, Institute of Plant Protection, Henan Provincial Academy of Agricultural Sciences – sequence: 2 givenname: Xiaojie surname: Li fullname: Li, Xiaojie organization: State Ministry of Education Key Laboratory of Integrated Management of Crop Pests, Nanjing Agricultural University – sequence: 3 givenname: Rong surname: Gao fullname: Gao, Rong organization: State Ministry of Education Key Laboratory of Integrated Management of Crop Pests, Nanjing Agricultural University – sequence: 4 givenname: Zhenzhen surname: You fullname: You, Zhenzhen organization: State Ministry of Education Key Laboratory of Integrated Management of Crop Pests, Nanjing Agricultural University – sequence: 5 givenname: Beibei surname: Lü fullname: Lü, Beibei organization: State Ministry of Education Key Laboratory of Integrated Management of Crop Pests, Nanjing Agricultural University – sequence: 6 givenname: Peiqing surname: Liu fullname: Liu, Peiqing organization: State Ministry of Education Key Laboratory of Integrated Management of Crop Pests, Nanjing Agricultural University – sequence: 7 givenname: Qixiang surname: Ma fullname: Ma, Qixiang organization: State Ministry of Education Key Laboratory of Integrated Management of Crop Pests, Nanjing Agricultural University, Institute of Plant Protection, Henan Provincial Academy of Agricultural Sciences – sequence: 8 givenname: Hansong surname: Dong fullname: Dong, Hansong email: hsdong@njau.edu.cn organization: State Ministry of Education Key Laboratory of Integrated Management of Crop Pests, Nanjing Agricultural University
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/22581008$$D View this record in MEDLINE/PubMed
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Snippet	Harpin proteins secreted by phytopathogenic bacteria have been shown to activate the plant defense pathway, which involves transduction of a hydrogen peroxide...
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SubjectTerms	Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis - microbiology Bacterial Outer Membrane Proteins - genetics Bacterial Outer Membrane Proteins - metabolism Biochemistry Biological Transport, Active Biomedical and Life Sciences Cell Membrane - metabolism Cytoplasm - metabolism Extracellular Space - metabolism Genes, Bacterial Hydrogen Peroxide - metabolism Life Sciences Plant Diseases - microbiology Plant Pathology Plant Sciences Plants, Genetically Modified Recombinant Proteins - genetics Recombinant Proteins - metabolism Xanthomonas - genetics Xanthomonas - metabolism Xanthomonas - pathogenicity
Title	Apoplastic and cytoplasmic location of harpin protein Hpa1Xoo plays different roles in H2O2 generation and pathogen resistance in Arabidopsis
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