Candidate pathogenicity factor/effector proteins of ‘Candidatus Phytoplasma solani’ modulate plant carbohydrate metabolism, accelerate the ascorbate–glutathione cycle, and induce autophagosomes
The pathogenicity of intracellular plant pathogenic bacteria is associated with the action of pathogenicity factors/effectors, but their physiological roles for most phytoplasma species, including ‘Candidiatus Phytoplasma solani’ are unknown. Six putative pathogenicity factors/effectors from six dif...
| Main Authors: | , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-08-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2023.1232367/full |
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| author | Marina Dermastia Špela Tomaž Špela Tomaž Rebeka Strah Rebeka Strah Tjaša Lukan Anna Coll Barbara Dušak Barbara Dušak Barbara Anžič Timotej Čepin Stefanie Wienkoop Aleš Kladnik Maja Zagorščak Monika Riedle-Bauer Christina Schönhuber Wolfram Weckwerth Wolfram Weckwerth Kristina Gruden Thomas Roitsch Maruša Pompe Novak Maruša Pompe Novak Günter Brader |
| author_facet | Marina Dermastia Špela Tomaž Špela Tomaž Rebeka Strah Rebeka Strah Tjaša Lukan Anna Coll Barbara Dušak Barbara Dušak Barbara Anžič Timotej Čepin Stefanie Wienkoop Aleš Kladnik Maja Zagorščak Monika Riedle-Bauer Christina Schönhuber Wolfram Weckwerth Wolfram Weckwerth Kristina Gruden Thomas Roitsch Maruša Pompe Novak Maruša Pompe Novak Günter Brader |
| author_sort | Marina Dermastia |
| collection | DOAJ |
| description | The pathogenicity of intracellular plant pathogenic bacteria is associated with the action of pathogenicity factors/effectors, but their physiological roles for most phytoplasma species, including ‘Candidiatus Phytoplasma solani’ are unknown. Six putative pathogenicity factors/effectors from six different strains of ‘Ca. P. solani’ were selected by bioinformatic analysis. The way in which they manipulate the host cellular machinery was elucidated by analyzing Nicotiana benthamiana leaves after Agrobacterium-mediated transient transformation with the pathogenicity factor/effector constructs using confocal microscopy, pull-down, and co-immunoprecipitation, and enzyme assays. Candidate pathogenicity factors/effectors were shown to modulate plant carbohydrate metabolism and the ascorbate–glutathione cycle and to induce autophagosomes. PoStoSP06, PoStoSP13, and PoStoSP28 were localized in the nucleus and cytosol. The most active effector in the processes studied was PoStoSP06. PoStoSP18 was associated with an increase in phosphoglucomutase activity, whereas PoStoSP28, previously annotated as an antigenic membrane protein StAMP, specifically interacted with phosphoglucomutase. PoStoSP04 induced only the ascorbate–glutathione cycle along with other pathogenicity factors/effectors. Candidate pathogenicity factors/effectors were involved in reprogramming host carbohydrate metabolism in favor of phytoplasma own growth and infection. They were specifically associated with three distinct metabolic pathways leading to fructose-6-phosphate as an input substrate for glycolysis. The possible significance of autophagosome induction by PoStoSP28 is discussed. |
| first_indexed | 2024-03-12T14:24:20Z |
| format | Article |
| id | doaj.art-6ada0b746d58449dab5934a112c05352 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-03-12T14:24:20Z |
| publishDate | 2023-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-6ada0b746d58449dab5934a112c053522023-08-18T11:18:27ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-08-011410.3389/fpls.2023.12323671232367Candidate pathogenicity factor/effector proteins of ‘Candidatus Phytoplasma solani’ modulate plant carbohydrate metabolism, accelerate the ascorbate–glutathione cycle, and induce autophagosomesMarina Dermastia0Špela Tomaž1Špela Tomaž2Rebeka Strah3Rebeka Strah4Tjaša Lukan5Anna Coll6Barbara Dušak7Barbara Dušak8Barbara Anžič9Timotej Čepin10Stefanie Wienkoop11Aleš Kladnik12Maja Zagorščak13Monika Riedle-Bauer14Christina Schönhuber15Wolfram Weckwerth16Wolfram Weckwerth17Kristina Gruden18Thomas Roitsch19Maruša Pompe Novak20Maruša Pompe Novak21Günter Brader22Department of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, SloveniaDepartment of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, SloveniaJožef Stefan International Postgraduate School, Ljubljana, SloveniaDepartment of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, SloveniaJožef Stefan International Postgraduate School, Ljubljana, SloveniaDepartment of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, SloveniaDepartment of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, SloveniaDepartment of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, SloveniaDepartment of Plant and Environmental Sciences, University of Copenhagen, Taastrup, DenmarkDepartment of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, SloveniaDepartment of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, SloveniaDepartment of Functional and Evolutionary Ecology, Faculty of Life Sciences, University of Vienna, Vienna, AustriaDepartment of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, SloveniaDepartment of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, SloveniaFederal College and Research Institute for Viticulture and Pomology Klosterneuburg, Klosterneuburg, AustriaBioresources Unit, Health & Environment Department, Austrian Institute of Technology, Tulln, AustriaDepartment of Functional and Evolutionary Ecology, Faculty of Life Sciences, University of Vienna, Vienna, AustriaVienna Metabolomics Center (VIME), University of Vienna, Vienna, AustriaDepartment of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, SloveniaDepartment of Plant and Environmental Sciences, University of Copenhagen, Taastrup, DenmarkDepartment of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, SloveniaFaculty of Viticulture and Enology, University of Nova Gorica, Vipava, SloveniaBioresources Unit, Health & Environment Department, Austrian Institute of Technology, Tulln, AustriaThe pathogenicity of intracellular plant pathogenic bacteria is associated with the action of pathogenicity factors/effectors, but their physiological roles for most phytoplasma species, including ‘Candidiatus Phytoplasma solani’ are unknown. Six putative pathogenicity factors/effectors from six different strains of ‘Ca. P. solani’ were selected by bioinformatic analysis. The way in which they manipulate the host cellular machinery was elucidated by analyzing Nicotiana benthamiana leaves after Agrobacterium-mediated transient transformation with the pathogenicity factor/effector constructs using confocal microscopy, pull-down, and co-immunoprecipitation, and enzyme assays. Candidate pathogenicity factors/effectors were shown to modulate plant carbohydrate metabolism and the ascorbate–glutathione cycle and to induce autophagosomes. PoStoSP06, PoStoSP13, and PoStoSP28 were localized in the nucleus and cytosol. The most active effector in the processes studied was PoStoSP06. PoStoSP18 was associated with an increase in phosphoglucomutase activity, whereas PoStoSP28, previously annotated as an antigenic membrane protein StAMP, specifically interacted with phosphoglucomutase. PoStoSP04 induced only the ascorbate–glutathione cycle along with other pathogenicity factors/effectors. Candidate pathogenicity factors/effectors were involved in reprogramming host carbohydrate metabolism in favor of phytoplasma own growth and infection. They were specifically associated with three distinct metabolic pathways leading to fructose-6-phosphate as an input substrate for glycolysis. The possible significance of autophagosome induction by PoStoSP28 is discussed.https://www.frontiersin.org/articles/10.3389/fpls.2023.1232367/fullautophagosome‘Candidatus Phytoplasma solani’effectorglycolysispathogenicity factorStAMP |
| spellingShingle | Marina Dermastia Špela Tomaž Špela Tomaž Rebeka Strah Rebeka Strah Tjaša Lukan Anna Coll Barbara Dušak Barbara Dušak Barbara Anžič Timotej Čepin Stefanie Wienkoop Aleš Kladnik Maja Zagorščak Monika Riedle-Bauer Christina Schönhuber Wolfram Weckwerth Wolfram Weckwerth Kristina Gruden Thomas Roitsch Maruša Pompe Novak Maruša Pompe Novak Günter Brader Candidate pathogenicity factor/effector proteins of ‘Candidatus Phytoplasma solani’ modulate plant carbohydrate metabolism, accelerate the ascorbate–glutathione cycle, and induce autophagosomes Frontiers in Plant Science autophagosome ‘Candidatus Phytoplasma solani’ effector glycolysis pathogenicity factor StAMP |
| title | Candidate pathogenicity factor/effector proteins of ‘Candidatus Phytoplasma solani’ modulate plant carbohydrate metabolism, accelerate the ascorbate–glutathione cycle, and induce autophagosomes |
| title_full | Candidate pathogenicity factor/effector proteins of ‘Candidatus Phytoplasma solani’ modulate plant carbohydrate metabolism, accelerate the ascorbate–glutathione cycle, and induce autophagosomes |
| title_fullStr | Candidate pathogenicity factor/effector proteins of ‘Candidatus Phytoplasma solani’ modulate plant carbohydrate metabolism, accelerate the ascorbate–glutathione cycle, and induce autophagosomes |
| title_full_unstemmed | Candidate pathogenicity factor/effector proteins of ‘Candidatus Phytoplasma solani’ modulate plant carbohydrate metabolism, accelerate the ascorbate–glutathione cycle, and induce autophagosomes |
| title_short | Candidate pathogenicity factor/effector proteins of ‘Candidatus Phytoplasma solani’ modulate plant carbohydrate metabolism, accelerate the ascorbate–glutathione cycle, and induce autophagosomes |
| title_sort | candidate pathogenicity factor effector proteins of candidatus phytoplasma solani modulate plant carbohydrate metabolism accelerate the ascorbate glutathione cycle and induce autophagosomes |
| topic | autophagosome ‘Candidatus Phytoplasma solani’ effector glycolysis pathogenicity factor StAMP |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2023.1232367/full |
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