Barley resistance and susceptibility to fungal cell entry involve the interplay of ROP signaling with phosphatidylinositol‐monophosphates
SUMMARY Rho‐of‐plant small GTPases (ROPs) are regulators of plant polar growth and of plant–pathogen interactions. The barley ROP, RACB, is involved in susceptibility toward infection by the barley powdery mildew fungus Blumeria hordei (Bh) but little is known about the cellular pathways that connec...
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| Vydané v: | The Plant journal : for cell and molecular biology Ročník 123; číslo 2; s. e70356 - n/a |
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| Hlavní autori: | , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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England
John Wiley and Sons Inc
01.07.2025
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| ISSN: | 0960-7412, 1365-313X, 1365-313X |
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| Abstract | SUMMARY
Rho‐of‐plant small GTPases (ROPs) are regulators of plant polar growth and of plant–pathogen interactions. The barley ROP, RACB, is involved in susceptibility toward infection by the barley powdery mildew fungus Blumeria hordei (Bh) but little is known about the cellular pathways that connect RACB signaling to disease susceptibility. Here we identify novel RACB interaction partners of plant or fungal origin by untargeted co‐immunoprecipitation of constitutively active (CA) RACB tagged by green fluorescent protein from Bh‐infected barley epidermal layers and subsequent analysis by liquid chromatography‐coupled mass spectrometry. Three of the immunoprecipitated proteins, a plant phosphoinositide phosphatase, a plant phosphoinositide phospholipase, and a putative Bh‐effector protein, are involved in the barley‐Bh‐pathosystem and support disease resistance or susceptibility, respectively. RACB and its plant interactors bind to overlapping anionic phospholipid species in vitro, and in the case of RACB, this lipid interaction is mediated by its carboxy‐terminal polybasic region (PBR). Fluorescent markers for anionic phospholipids show altered subcellular distribution in barley cells during Bh attack and under expression of a RACB‐binding fungal effector. Phosphatidylinositol 4‐phosphate, phosphatidylinositol 3,5‐bisphosphate, and phosphatidylserine show a distinct enrichment at the haustorial neck region, suggesting a connection to subcellular targeting of RACB at this site. The interplay of ROPs with anionic phospholipids and phospholipid‐metabolizing enzymes may thus enable the subcellular enrichment of components pivotal for success or failure of fungal penetration.
Significance Statement
The ROP GTPase RACB has been co‐immunoprecipitated with two host phospholipid‐metabolizing enzymes and one fungal effector that influences pathogen interaction. All three modeled protein complexes share an overlapping binding interface with RACB.
Rho‐of‐plant small GTPases (ROPs) are regulators of plant cell polarity, disease resistance, and susceptibility to fungal invasion of plant cells. In cell development, ROPs act in concert with phosphoinositides, but such a function was not established for ROP signaling in plant–microbe interactions. Here we show relevant phosphoinositide interaction of barley RACB, a ROP GTPase acting in susceptibility to invasion by Blumeria hordei, and new interaction partners of RACB that influence fungal invasion success and may act on plant phosphoinositide metabolism. |
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| AbstractList | Rho‐of‐plant small GTPases (ROPs) are regulators of plant polar growth and of plant–pathogen interactions. The barley ROP, RACB, is involved in susceptibility toward infection by the barley powdery mildew fungus Blumeria hordei ( Bh ) but little is known about the cellular pathways that connect RACB signaling to disease susceptibility. Here we identify novel RACB interaction partners of plant or fungal origin by untargeted co‐immunoprecipitation of constitutively active (CA) RACB tagged by green fluorescent protein from Bh ‐infected barley epidermal layers and subsequent analysis by liquid chromatography‐coupled mass spectrometry. Three of the immunoprecipitated proteins, a plant phosphoinositide phosphatase, a plant phosphoinositide phospholipase, and a putative Bh ‐effector protein, are involved in the barley‐ Bh‐ pathosystem and support disease resistance or susceptibility, respectively. RACB and its plant interactors bind to overlapping anionic phospholipid species in vitro , and in the case of RACB, this lipid interaction is mediated by its carboxy‐terminal polybasic region (PBR). Fluorescent markers for anionic phospholipids show altered subcellular distribution in barley cells during Bh attack and under expression of a RACB‐binding fungal effector. Phosphatidylinositol 4‐phosphate, phosphatidylinositol 3,5‐bisphosphate, and phosphatidylserine show a distinct enrichment at the haustorial neck region, suggesting a connection to subcellular targeting of RACB at this site. The interplay of ROPs with anionic phospholipids and phospholipid‐metabolizing enzymes may thus enable the subcellular enrichment of components pivotal for success or failure of fungal penetration. Rho‐of‐plant small GTPases (ROPs) are regulators of plant polar growth and of plant–pathogen interactions. The barley ROP, RACB, is involved in susceptibility toward infection by the barley powdery mildew fungus Blumeria hordei (Bh) but little is known about the cellular pathways that connect RACB signaling to disease susceptibility. Here we identify novel RACB interaction partners of plant or fungal origin by untargeted co‐immunoprecipitation of constitutively active (CA) RACB tagged by green fluorescent protein from Bh‐infected barley epidermal layers and subsequent analysis by liquid chromatography‐coupled mass spectrometry. Three of the immunoprecipitated proteins, a plant phosphoinositide phosphatase, a plant phosphoinositide phospholipase, and a putative Bh‐effector protein, are involved in the barley‐Bh‐pathosystem and support disease resistance or susceptibility, respectively. RACB and its plant interactors bind to overlapping anionic phospholipid species in vitro, and in the case of RACB, this lipid interaction is mediated by its carboxy‐terminal polybasic region (PBR). Fluorescent markers for anionic phospholipids show altered subcellular distribution in barley cells during Bh attack and under expression of a RACB‐binding fungal effector. Phosphatidylinositol 4‐phosphate, phosphatidylinositol 3,5‐bisphosphate, and phosphatidylserine show a distinct enrichment at the haustorial neck region, suggesting a connection to subcellular targeting of RACB at this site. The interplay of ROPs with anionic phospholipids and phospholipid‐metabolizing enzymes may thus enable the subcellular enrichment of components pivotal for success or failure of fungal penetration. The ROP GTPase RACB has been co‐immunoprecipitated with two host phospholipid‐metabolizing enzymes and one fungal effector that influences pathogen interaction. All three modeled protein complexes share an overlapping binding interface with RACB. Rho‐of‐plant small GTPases (ROPs) are regulators of plant cell polarity, disease resistance, and susceptibility to fungal invasion of plant cells. In cell development, ROPs act in concert with phosphoinositides, but such a function was not established for ROP signaling in plant–microbe interactions. Here we show relevant phosphoinositide interaction of barley RACB, a ROP GTPase acting in susceptibility to invasion by Blumeria hordei, and new interaction partners of RACB that influence fungal invasion success and may act on plant phosphoinositide metabolism. SUMMARY Rho‐of‐plant small GTPases (ROPs) are regulators of plant polar growth and of plant–pathogen interactions. The barley ROP, RACB, is involved in susceptibility toward infection by the barley powdery mildew fungus Blumeria hordei (Bh) but little is known about the cellular pathways that connect RACB signaling to disease susceptibility. Here we identify novel RACB interaction partners of plant or fungal origin by untargeted co‐immunoprecipitation of constitutively active (CA) RACB tagged by green fluorescent protein from Bh‐infected barley epidermal layers and subsequent analysis by liquid chromatography‐coupled mass spectrometry. Three of the immunoprecipitated proteins, a plant phosphoinositide phosphatase, a plant phosphoinositide phospholipase, and a putative Bh‐effector protein, are involved in the barley‐Bh‐pathosystem and support disease resistance or susceptibility, respectively. RACB and its plant interactors bind to overlapping anionic phospholipid species in vitro, and in the case of RACB, this lipid interaction is mediated by its carboxy‐terminal polybasic region (PBR). Fluorescent markers for anionic phospholipids show altered subcellular distribution in barley cells during Bh attack and under expression of a RACB‐binding fungal effector. Phosphatidylinositol 4‐phosphate, phosphatidylinositol 3,5‐bisphosphate, and phosphatidylserine show a distinct enrichment at the haustorial neck region, suggesting a connection to subcellular targeting of RACB at this site. The interplay of ROPs with anionic phospholipids and phospholipid‐metabolizing enzymes may thus enable the subcellular enrichment of components pivotal for success or failure of fungal penetration. Significance Statement The ROP GTPase RACB has been co‐immunoprecipitated with two host phospholipid‐metabolizing enzymes and one fungal effector that influences pathogen interaction. All three modeled protein complexes share an overlapping binding interface with RACB. Rho‐of‐plant small GTPases (ROPs) are regulators of plant cell polarity, disease resistance, and susceptibility to fungal invasion of plant cells. In cell development, ROPs act in concert with phosphoinositides, but such a function was not established for ROP signaling in plant–microbe interactions. Here we show relevant phosphoinositide interaction of barley RACB, a ROP GTPase acting in susceptibility to invasion by Blumeria hordei, and new interaction partners of RACB that influence fungal invasion success and may act on plant phosphoinositide metabolism. Rho-of-plant small GTPases (ROPs) are regulators of plant polar growth and of plant-pathogen interactions. The barley ROP, RACB, is involved in susceptibility toward infection by the barley powdery mildew fungus Blumeria hordei (Bh) but little is known about the cellular pathways that connect RACB signaling to disease susceptibility. Here we identify novel RACB interaction partners of plant or fungal origin by untargeted co-immunoprecipitation of constitutively active (CA) RACB tagged by green fluorescent protein from Bh-infected barley epidermal layers and subsequent analysis by liquid chromatography-coupled mass spectrometry. Three of the immunoprecipitated proteins, a plant phosphoinositide phosphatase, a plant phosphoinositide phospholipase, and a putative Bh-effector protein, are involved in the barley-Bh-pathosystem and support disease resistance or susceptibility, respectively. RACB and its plant interactors bind to overlapping anionic phospholipid species in vitro, and in the case of RACB, this lipid interaction is mediated by its carboxy-terminal polybasic region (PBR). Fluorescent markers for anionic phospholipids show altered subcellular distribution in barley cells during Bh attack and under expression of a RACB-binding fungal effector. Phosphatidylinositol 4-phosphate, phosphatidylinositol 3,5-bisphosphate, and phosphatidylserine show a distinct enrichment at the haustorial neck region, suggesting a connection to subcellular targeting of RACB at this site. The interplay of ROPs with anionic phospholipids and phospholipid-metabolizing enzymes may thus enable the subcellular enrichment of components pivotal for success or failure of fungal penetration.Rho-of-plant small GTPases (ROPs) are regulators of plant polar growth and of plant-pathogen interactions. The barley ROP, RACB, is involved in susceptibility toward infection by the barley powdery mildew fungus Blumeria hordei (Bh) but little is known about the cellular pathways that connect RACB signaling to disease susceptibility. Here we identify novel RACB interaction partners of plant or fungal origin by untargeted co-immunoprecipitation of constitutively active (CA) RACB tagged by green fluorescent protein from Bh-infected barley epidermal layers and subsequent analysis by liquid chromatography-coupled mass spectrometry. Three of the immunoprecipitated proteins, a plant phosphoinositide phosphatase, a plant phosphoinositide phospholipase, and a putative Bh-effector protein, are involved in the barley-Bh-pathosystem and support disease resistance or susceptibility, respectively. RACB and its plant interactors bind to overlapping anionic phospholipid species in vitro, and in the case of RACB, this lipid interaction is mediated by its carboxy-terminal polybasic region (PBR). Fluorescent markers for anionic phospholipids show altered subcellular distribution in barley cells during Bh attack and under expression of a RACB-binding fungal effector. Phosphatidylinositol 4-phosphate, phosphatidylinositol 3,5-bisphosphate, and phosphatidylserine show a distinct enrichment at the haustorial neck region, suggesting a connection to subcellular targeting of RACB at this site. The interplay of ROPs with anionic phospholipids and phospholipid-metabolizing enzymes may thus enable the subcellular enrichment of components pivotal for success or failure of fungal penetration. |
| Author | Heilmann, Mareike Weiß, Lukas Sebastian Engelhardt, Stefan Heilmann, Ingo Hensel, Götz Mergner, Julia Bradai, Mariem Bartram, Christoph Kumlehn, Jochen Hückelhoven, Ralph Kuster, Bernhard |
| AuthorAffiliation | 2 Department of Plant Biochemistry, Institute of Biochemistry and Biotechnology Martin‐Luther‐University Halle‐Wittenberg Halle (Saale) Germany 4 Bavarian Biomolecular Mass Spectrometry Center (BayBioMS) Technical University of Munich Freising Germany 1 Chair of Phytopathology, TUM School of Life Sciences Technical University of Munich Freising Germany 5 Institute of Plant Genetics and Crop Plant Research Gatersleben Germany 3 Chair of Proteomics and Bioanalytics Technical University of Munich Freising Germany 6 Heinrich Heine University Düsseldorf, Faculty of Mathematics and Natural Sciences Centre for Plant Genome Engineering Düsseldorf Germany |
| AuthorAffiliation_xml | – name: 6 Heinrich Heine University Düsseldorf, Faculty of Mathematics and Natural Sciences Centre for Plant Genome Engineering Düsseldorf Germany – name: 5 Institute of Plant Genetics and Crop Plant Research Gatersleben Germany – name: 1 Chair of Phytopathology, TUM School of Life Sciences Technical University of Munich Freising Germany – name: 4 Bavarian Biomolecular Mass Spectrometry Center (BayBioMS) Technical University of Munich Freising Germany – name: 2 Department of Plant Biochemistry, Institute of Biochemistry and Biotechnology Martin‐Luther‐University Halle‐Wittenberg Halle (Saale) Germany – name: 3 Chair of Proteomics and Bioanalytics Technical University of Munich Freising Germany |
| Author_xml | – sequence: 1 givenname: Lukas Sebastian surname: Weiß fullname: Weiß, Lukas Sebastian organization: Technical University of Munich – sequence: 2 givenname: Mariem orcidid: 0000-0002-0474-220X surname: Bradai fullname: Bradai, Mariem organization: Technical University of Munich – sequence: 3 givenname: Christoph surname: Bartram fullname: Bartram, Christoph organization: Technical University of Munich – sequence: 4 givenname: Mareike orcidid: 0000-0002-0929-9374 surname: Heilmann fullname: Heilmann, Mareike organization: Martin‐Luther‐University Halle‐Wittenberg – sequence: 5 givenname: Julia orcidid: 0000-0002-4332-1280 surname: Mergner fullname: Mergner, Julia organization: Technical University of Munich – sequence: 6 givenname: Bernhard orcidid: 0000-0002-9094-1677 surname: Kuster fullname: Kuster, Bernhard organization: Technical University of Munich – sequence: 7 givenname: Götz orcidid: 0000-0002-5539-3097 surname: Hensel fullname: Hensel, Götz organization: Centre for Plant Genome Engineering – sequence: 8 givenname: Jochen orcidid: 0000-0001-7080-7983 surname: Kumlehn fullname: Kumlehn, Jochen organization: Institute of Plant Genetics and Crop Plant Research – sequence: 9 givenname: Stefan orcidid: 0000-0003-1933-1160 surname: Engelhardt fullname: Engelhardt, Stefan organization: Technical University of Munich – sequence: 10 givenname: Ingo orcidid: 0000-0002-2324-1849 surname: Heilmann fullname: Heilmann, Ingo organization: Martin‐Luther‐University Halle‐Wittenberg – sequence: 11 givenname: Ralph orcidid: 0000-0001-5632-5451 surname: Hückelhoven fullname: Hückelhoven, Ralph email: hueckelhoven@tum.de organization: Technical University of Munich |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/40680717$$D View this record in MEDLINE/PubMed |
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Rho‐of‐plant small GTPases (ROPs) are regulators of plant polar growth and of plant–pathogen interactions. The barley ROP, RACB, is involved in... Rho‐of‐plant small GTPases (ROPs) are regulators of plant polar growth and of plant–pathogen interactions. The barley ROP, RACB, is involved in susceptibility... Rho-of-plant small GTPases (ROPs) are regulators of plant polar growth and of plant-pathogen interactions. The barley ROP, RACB, is involved in susceptibility... |
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| StartPage | e70356 |
| SubjectTerms | Ascomycota - pathogenicity Ascomycota - physiology barley Blumeria Disease Resistance disease susceptibility effector fluorescence fungi green fluorescent protein guanosinetriphosphatase haustoria haustorium Hordeum - genetics Hordeum - immunology Hordeum - metabolism Hordeum - microbiology Host-Pathogen Interactions mass spectrometry neck Original Phosphatidylinositol Phosphates - metabolism phosphatidylinositol‐monophosphate phosphatidylserines phosphoinositide phosphatase phosphoinositide phospholipase phospholipases Plant Diseases - immunology Plant Diseases - microbiology Plant Proteins - genetics Plant Proteins - metabolism polarity polybasic domain powdery mildew precipitin tests ROP GTPAse Signal Transduction species susceptibility |
| Title | Barley resistance and susceptibility to fungal cell entry involve the interplay of ROP signaling with phosphatidylinositol‐monophosphates |
| URI | https://onlinelibrary.wiley.com/doi/abs/10.1111%2Ftpj.70356 https://www.ncbi.nlm.nih.gov/pubmed/40680717 https://www.proquest.com/docview/3231645413 https://www.proquest.com/docview/3242085412 https://pubmed.ncbi.nlm.nih.gov/PMC12274078 |
| Volume | 123 |
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