Cytokinin production by Pseudomonas fluorescens G20-18 determines biocontrol activity against Pseudomonas syringae in Arabidopsis

Plant beneficial microbes mediate biocontrol of diseases by interfering with pathogens or via strengthening the host. Although phytohormones, including cytokinins, are known to regulate plant development and physiology as well as plant immunity, their production by microorganisms has not been consid...

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Published in	Scientific reports Vol. 6; no. 1; p. 23310
Main Authors	Großkinsky, Dominik K., Tafner, Richard, Moreno, María V., Stenglein, Sebastian A., García de Salamone, Inés E., Nelson, Louise M., Novák, Ondřej, Strnad, Miroslav, van der Graaff, Eric, Roitsch, Thomas
Format	Journal Article
Language	English
Published	London Nature Publishing Group UK 17.03.2016 Nature Publishing Group
Subjects	631/449/1741/1406 631/449/2169/2674 631/449/2661/2666 Abiotic stress Arabidopsis - microbiology Biological control Biomass Cell division Chromatography, High Pressure Liquid Complementation Cytokinins Cytokinins - analysis Cytokinins - biosynthesis Cytokinins - pharmacology Gene expression Host plants Humanities and Social Sciences Infections Microorganisms multidisciplinary Pathogens Physiology Plant diseases Plant Diseases - microbiology Plant Growth Regulators - pharmacology Plant hormones Plant immunity Plant Leaves - microbiology Plant protection Plant resistance Pseudomonas fluorescens - metabolism Pseudomonas syringae - drug effects Pseudomonas syringae - growth & development Pseudomonas syringae - pathogenicity Salicylic acid Salicylic Acid - pharmacology Science Tandem Mass Spectrometry
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Abstract	Plant beneficial microbes mediate biocontrol of diseases by interfering with pathogens or via strengthening the host. Although phytohormones, including cytokinins, are known to regulate plant development and physiology as well as plant immunity, their production by microorganisms has not been considered as a biocontrol mechanism. Here we identify the ability of Pseudomonas fluorescens G20-18 to efficiently control P. syringae infection in Arabidopsis , allowing maintenance of tissue integrity and ultimately biomass yield. Microbial cytokinin production was identified as a key determinant for this biocontrol effect on the hemibiotrophic bacterial pathogen. While cytokinin-deficient loss-of-function mutants of G20-18 exhibit impaired biocontrol, functional complementation with cytokinin biosynthetic genes restores cytokinin-mediated biocontrol, which is correlated with differential cytokinin levels in planta . Arabidopsis mutant analyses revealed the necessity of functional plant cytokinin perception and salicylic acid-dependent defence signalling for this biocontrol mechanism. These results demonstrate microbial cytokinin production as a novel microbe-based, hormone-mediated concept of biocontrol. This mechanism provides a basis to potentially develop novel, integrated plant protection strategies combining promotion of growth, a favourable physiological status and activation of fine-tuned direct defence and abiotic stress resilience.
AbstractList	Plant beneficial microbes mediate biocontrol of diseases by interfering with pathogens or via strengthening the host. Although phytohormones, including cytokinins, are known to regulate plant development and physiology as well as plant immunity, their production by microorganisms has not been considered as a biocontrol mechanism. Here we identify the ability of Pseudomonas fluorescens G20-18 to efficiently control P. syringae infection in Arabidopsis, allowing maintenance of tissue integrity and ultimately biomass yield. Microbial cytokinin production was identified as a key determinant for this biocontrol effect on the hemibiotrophic bacterial pathogen. While cytokinin-deficient loss-of-function mutants of G20-18 exhibit impaired biocontrol, functional complementation with cytokinin biosynthetic genes restores cytokinin-mediated biocontrol, which is correlated with differential cytokinin levels in planta. Arabidopsis mutant analyses revealed the necessity of functional plant cytokinin perception and salicylic acid-dependent defence signalling for this biocontrol mechanism. These results demonstrate microbial cytokinin production as a novel microbe-based, hormone-mediated concept of biocontrol. This mechanism provides a basis to potentially develop novel, integrated plant protection strategies combining promotion of growth, a favourable physiological status and activation of fine-tuned direct defence and abiotic stress resilience.Plant beneficial microbes mediate biocontrol of diseases by interfering with pathogens or via strengthening the host. Although phytohormones, including cytokinins, are known to regulate plant development and physiology as well as plant immunity, their production by microorganisms has not been considered as a biocontrol mechanism. Here we identify the ability of Pseudomonas fluorescens G20-18 to efficiently control P. syringae infection in Arabidopsis, allowing maintenance of tissue integrity and ultimately biomass yield. Microbial cytokinin production was identified as a key determinant for this biocontrol effect on the hemibiotrophic bacterial pathogen. While cytokinin-deficient loss-of-function mutants of G20-18 exhibit impaired biocontrol, functional complementation with cytokinin biosynthetic genes restores cytokinin-mediated biocontrol, which is correlated with differential cytokinin levels in planta. Arabidopsis mutant analyses revealed the necessity of functional plant cytokinin perception and salicylic acid-dependent defence signalling for this biocontrol mechanism. These results demonstrate microbial cytokinin production as a novel microbe-based, hormone-mediated concept of biocontrol. This mechanism provides a basis to potentially develop novel, integrated plant protection strategies combining promotion of growth, a favourable physiological status and activation of fine-tuned direct defence and abiotic stress resilience. Plant beneficial microbes mediate biocontrol of diseases by interfering with pathogens or via strengthening the host. Although phytohormones, including cytokinins, are known to regulate plant development and physiology as well as plant immunity, their production by microorganisms has not been considered as a biocontrol mechanism. Here we identify the ability of Pseudomonas fluorescens G20-18 to efficiently control P. syringae infection in Arabidopsis, allowing maintenance of tissue integrity and ultimately biomass yield. Microbial cytokinin production was identified as a key determinant for this biocontrol effect on the hemibiotrophic bacterial pathogen. While cytokinin-deficient loss-of-function mutants of G20-18 exhibit impaired biocontrol, functional complementation with cytokinin biosynthetic genes restores cytokinin-mediated biocontrol, which is correlated with differential cytokinin levels in planta. Arabidopsis mutant analyses revealed the necessity of functional plant cytokinin perception and salicylic acid-dependent defence signalling for this biocontrol mechanism. These results demonstrate microbial cytokinin production as a novel microbe-based, hormone-mediated concept of biocontrol. This mechanism provides a basis to potentially develop novel, integrated plant protection strategies combining promotion of growth, a favourable physiological status and activation of fine-tuned direct defence and abiotic stress resilience. Plant beneficial microbes mediate biocontrol of diseases by interfering with pathogens or via strengthening the host. Although phytohormones, including cytokinins, are known to regulate plant development and physiology as well as plant immunity, their production by microorganisms has not been considered as a biocontrol mechanism. Here we identify the ability of Pseudomonas fluorescens G20-18 to efficiently control P. syringae infection in Arabidopsis , allowing maintenance of tissue integrity and ultimately biomass yield. Microbial cytokinin production was identified as a key determinant for this biocontrol effect on the hemibiotrophic bacterial pathogen. While cytokinin-deficient loss-of-function mutants of G20-18 exhibit impaired biocontrol, functional complementation with cytokinin biosynthetic genes restores cytokinin-mediated biocontrol, which is correlated with differential cytokinin levels in planta . Arabidopsis mutant analyses revealed the necessity of functional plant cytokinin perception and salicylic acid-dependent defence signalling for this biocontrol mechanism. These results demonstrate microbial cytokinin production as a novel microbe-based, hormone-mediated concept of biocontrol. This mechanism provides a basis to potentially develop novel, integrated plant protection strategies combining promotion of growth, a favourable physiological status and activation of fine-tuned direct defence and abiotic stress resilience.
ArticleNumber	23310
Author	Novák, Ondřej Großkinsky, Dominik K. Strnad, Miroslav Roitsch, Thomas Tafner, Richard Nelson, Louise M. Moreno, María V. García de Salamone, Inés E. van der Graaff, Eric Stenglein, Sebastian A.
Author_xml	– sequence: 1 givenname: Dominik K. surname: Großkinsky fullname: Großkinsky, Dominik K. organization: Department of Plant and Environmental Sciences, Copenhagen Plant Science Centre, University of Copenhagen, Department of Plant Physiology, Institute of Plant Sciences, University of Graz – sequence: 2 givenname: Richard surname: Tafner fullname: Tafner, Richard organization: Department of Plant Physiology, Institute of Plant Sciences, University of Graz – sequence: 3 givenname: María V. surname: Moreno fullname: Moreno, María V. organization: Department of Plant Physiology, Institute of Plant Sciences, University of Graz, Laboratorio de Biología Funcional y Biotecnología (BIOLAB)-CICBA-INBIOTEC-CONICET, Facultad de Agronomía de Azul-UNCPBA, Cátedra de Microbiología, Facultad de Agronomía de Azul-UNCPBA – sequence: 4 givenname: Sebastian A. surname: Stenglein fullname: Stenglein, Sebastian A. organization: Department of Plant Physiology, Institute of Plant Sciences, University of Graz, Laboratorio de Biología Funcional y Biotecnología (BIOLAB)-CICBA-INBIOTEC-CONICET, Facultad de Agronomía de Azul-UNCPBA, Cátedra de Microbiología, Facultad de Agronomía de Azul-UNCPBA – sequence: 5 givenname: Inés E. surname: García de Salamone fullname: García de Salamone, Inés E. organization: Cátedra de Microbiología Agrícola, Facultad de Agronomía, Universidad de Buenos Aires – sequence: 6 givenname: Louise M. surname: Nelson fullname: Nelson, Louise M. organization: Department of Biology, Irving K Barber School of Arts and Sciences, University of British Columbia Okanagan Campus – sequence: 7 givenname: Ondřej surname: Novák fullname: Novák, Ondřej organization: Laboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany ASCR & Faculty of Science, Palacký University – sequence: 8 givenname: Miroslav surname: Strnad fullname: Strnad, Miroslav organization: Laboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany ASCR & Faculty of Science, Palacký University – sequence: 9 givenname: Eric surname: van der Graaff fullname: van der Graaff, Eric organization: Department of Plant and Environmental Sciences, Copenhagen Plant Science Centre, University of Copenhagen, Department of Plant Physiology, Institute of Plant Sciences, University of Graz – sequence: 10 givenname: Thomas surname: Roitsch fullname: Roitsch, Thomas organization: Department of Plant and Environmental Sciences, Copenhagen Plant Science Centre, University of Copenhagen, Department of Plant Physiology, Institute of Plant Sciences, University of Graz, Global Change Research Centre, Czech Globe AS CR
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SubjectTerms	631/449/1741/1406 631/449/2169/2674 631/449/2661/2666 Abiotic stress Arabidopsis - microbiology Biological control Biomass Cell division Chromatography, High Pressure Liquid Complementation Cytokinins Cytokinins - analysis Cytokinins - biosynthesis Cytokinins - pharmacology Gene expression Host plants Humanities and Social Sciences Infections Microorganisms multidisciplinary Pathogens Physiology Plant diseases Plant Diseases - microbiology Plant Growth Regulators - pharmacology Plant hormones Plant immunity Plant Leaves - microbiology Plant protection Plant resistance Pseudomonas fluorescens - metabolism Pseudomonas syringae - drug effects Pseudomonas syringae - growth & development Pseudomonas syringae - pathogenicity Salicylic acid Salicylic Acid - pharmacology Science Tandem Mass Spectrometry
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Title	Cytokinin production by Pseudomonas fluorescens G20-18 determines biocontrol activity against Pseudomonas syringae in Arabidopsis
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