Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling

Dominik Kilian Grosskinsky; Muhammad Naseem; Usama Ramadan Abdelmohsen; Nicole Plickert; Thomas Engelke; Thomas Griebel; Juergen Zeier; Ondrej Novak; Miroslav Strnad; Hartwig Pfeifhofer; Eric van der Graaff; Uwe Simon; Thomas Georg Roitsch

doi:10.1104/pp.111.182931

Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling

Dominik Kilian Grosskinsky, Muhammad Naseem, Usama Ramadan Abdelmohsen, Nicole Plickert, Thomas Engelke, Thomas Griebel, Juergen Zeier, Ondrej Novak, Miroslav Strnad, Hartwig Pfeifhofer, Eric van der Graaff, Uwe Simon, Thomas Georg Roitsch

111 Citations (Scopus)

Abstract

Cytokinins are phytohormones that are involved in various regulatory processes throughout plant development, but they are also produced by pathogens and known to modulate plant immunity. A novel transgenic approach enabling autoregulated cytokinin synthesis in response to pathogen infection showed that cytokinins mediate enhanced resistance against the virulent hemibiotrophic pathogen Pseudomonas syringae pv tabaci. This was confirmed by two additional independent transgenic approaches to increase endogenous cytokinin production and by exogenous supply of adenine-and phenylurea-derived cytokinins. The cytokinin-mediated resistance strongly correlated with an increased level of bactericidal activities and up-regulated synthesis of the two major antimicrobial phytoalexins in tobacco (Nicotiana tabacum), scopoletin and capsidiol. The key role of these phytoalexins in the underlying mechanism was functionally proven by the finding that scopoletin and capsidiol substitute in planta for the cytokinin signal: phytoalexin pretreatment increased resistance against P. syringae. In contrast to a cytokinin defense mechanism in Arabidopsis (Arabidopsis thaliana) based on salicylic acid-dependent transcriptional control, the cytokininmediated resistance in tobacco is essentially independent from salicylic acid and differs in pathogen specificity. It is also independent of jasmonate levels, reactive oxygen species, and high sugar resistance. The novel function of cytokinins in the primary defense response of solanaceous plant species is rather mediated through a high phytoalexin-pathogen ratio in the early phase of infection, which efficiently restricts pathogen growth. The implications of this mechanism for the coevolution of host plants and cytokinin-producing pathogens and the practical application in agriculture are discussed.

Original language	English
Journal	Plant Physiology
Volume	157
Issue number	2
Pages (from-to)	815-830
Number of pages	16
ISSN	0032-0889
DOIs	https://doi.org/10.1104/pp.111.182931
Publication status	Published - Oct 2011
Externally published	Yes

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Grosskinsky, D. K., Naseem, M., Abdelmohsen, U. R., Plickert, N., Engelke, T., Griebel, T., Zeier, J., Novak, O., Strnad, M., Pfeifhofer, H., van der Graaff, E., Simon, U., & Roitsch, T. G. (2011). Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling. Plant Physiology, 157(2), 815-830. https://doi.org/10.1104/pp.111.182931

Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling. / Grosskinsky, Dominik Kilian; Naseem, Muhammad; Abdelmohsen, Usama Ramadan et al.

In: Plant Physiology, Vol. 157, No. 2, 10.2011, p. 815-830.

Research output: Contribution to journal › Journal article › Research › peer-review

Grosskinsky, DK, Naseem, M, Abdelmohsen, UR, Plickert, N, Engelke, T, Griebel, T, Zeier, J, Novak, O, Strnad, M, Pfeifhofer, H, van der Graaff, E, Simon, U & Roitsch, TG 2011, 'Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling', Plant Physiology, vol. 157, no. 2, pp. 815-830. https://doi.org/10.1104/pp.111.182931

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title = "Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling",

abstract = "Cytokinins are phytohormones that are involved in various regulatory processes throughout plant development, but they are also produced by pathogens and known to modulate plant immunity. A novel transgenic approach enabling autoregulated cytokinin synthesis in response to pathogen infection showed that cytokinins mediate enhanced resistance against the virulent hemibiotrophic pathogen Pseudomonas syringae pv tabaci. This was confirmed by two additional independent transgenic approaches to increase endogenous cytokinin production and by exogenous supply of adenine-and phenylurea-derived cytokinins. The cytokinin-mediated resistance strongly correlated with an increased level of bactericidal activities and up-regulated synthesis of the two major antimicrobial phytoalexins in tobacco (Nicotiana tabacum), scopoletin and capsidiol. The key role of these phytoalexins in the underlying mechanism was functionally proven by the finding that scopoletin and capsidiol substitute in planta for the cytokinin signal: phytoalexin pretreatment increased resistance against P. syringae. In contrast to a cytokinin defense mechanism in Arabidopsis (Arabidopsis thaliana) based on salicylic acid-dependent transcriptional control, the cytokininmediated resistance in tobacco is essentially independent from salicylic acid and differs in pathogen specificity. It is also independent of jasmonate levels, reactive oxygen species, and high sugar resistance. The novel function of cytokinins in the primary defense response of solanaceous plant species is rather mediated through a high phytoalexin-pathogen ratio in the early phase of infection, which efficiently restricts pathogen growth. The implications of this mechanism for the coevolution of host plants and cytokinin-producing pathogens and the practical application in agriculture are discussed.",

author = "Grosskinsky, {Dominik Kilian} and Muhammad Naseem and Abdelmohsen, {Usama Ramadan} and Nicole Plickert and Thomas Engelke and Thomas Griebel and Juergen Zeier and Ondrej Novak and Miroslav Strnad and Hartwig Pfeifhofer and {van der Graaff}, Eric and Uwe Simon and Roitsch, {Thomas Georg}",

year = "2011",

month = oct,

doi = "10.1104/pp.111.182931",

language = "English",

volume = "157",

pages = "815--830",

journal = "Plant Physiology",

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publisher = "American Society of Plant Biologists",

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T1 - Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling

AU - Grosskinsky, Dominik Kilian

AU - Naseem, Muhammad

AU - Abdelmohsen, Usama Ramadan

AU - Plickert, Nicole

AU - Engelke, Thomas

AU - Griebel, Thomas

AU - Zeier, Juergen

AU - Novak, Ondrej

AU - Strnad, Miroslav

AU - Pfeifhofer, Hartwig

AU - van der Graaff, Eric

AU - Simon, Uwe

AU - Roitsch, Thomas Georg

PY - 2011/10

Y1 - 2011/10

N2 - Cytokinins are phytohormones that are involved in various regulatory processes throughout plant development, but they are also produced by pathogens and known to modulate plant immunity. A novel transgenic approach enabling autoregulated cytokinin synthesis in response to pathogen infection showed that cytokinins mediate enhanced resistance against the virulent hemibiotrophic pathogen Pseudomonas syringae pv tabaci. This was confirmed by two additional independent transgenic approaches to increase endogenous cytokinin production and by exogenous supply of adenine-and phenylurea-derived cytokinins. The cytokinin-mediated resistance strongly correlated with an increased level of bactericidal activities and up-regulated synthesis of the two major antimicrobial phytoalexins in tobacco (Nicotiana tabacum), scopoletin and capsidiol. The key role of these phytoalexins in the underlying mechanism was functionally proven by the finding that scopoletin and capsidiol substitute in planta for the cytokinin signal: phytoalexin pretreatment increased resistance against P. syringae. In contrast to a cytokinin defense mechanism in Arabidopsis (Arabidopsis thaliana) based on salicylic acid-dependent transcriptional control, the cytokininmediated resistance in tobacco is essentially independent from salicylic acid and differs in pathogen specificity. It is also independent of jasmonate levels, reactive oxygen species, and high sugar resistance. The novel function of cytokinins in the primary defense response of solanaceous plant species is rather mediated through a high phytoalexin-pathogen ratio in the early phase of infection, which efficiently restricts pathogen growth. The implications of this mechanism for the coevolution of host plants and cytokinin-producing pathogens and the practical application in agriculture are discussed.

AB - Cytokinins are phytohormones that are involved in various regulatory processes throughout plant development, but they are also produced by pathogens and known to modulate plant immunity. A novel transgenic approach enabling autoregulated cytokinin synthesis in response to pathogen infection showed that cytokinins mediate enhanced resistance against the virulent hemibiotrophic pathogen Pseudomonas syringae pv tabaci. This was confirmed by two additional independent transgenic approaches to increase endogenous cytokinin production and by exogenous supply of adenine-and phenylurea-derived cytokinins. The cytokinin-mediated resistance strongly correlated with an increased level of bactericidal activities and up-regulated synthesis of the two major antimicrobial phytoalexins in tobacco (Nicotiana tabacum), scopoletin and capsidiol. The key role of these phytoalexins in the underlying mechanism was functionally proven by the finding that scopoletin and capsidiol substitute in planta for the cytokinin signal: phytoalexin pretreatment increased resistance against P. syringae. In contrast to a cytokinin defense mechanism in Arabidopsis (Arabidopsis thaliana) based on salicylic acid-dependent transcriptional control, the cytokininmediated resistance in tobacco is essentially independent from salicylic acid and differs in pathogen specificity. It is also independent of jasmonate levels, reactive oxygen species, and high sugar resistance. The novel function of cytokinins in the primary defense response of solanaceous plant species is rather mediated through a high phytoalexin-pathogen ratio in the early phase of infection, which efficiently restricts pathogen growth. The implications of this mechanism for the coevolution of host plants and cytokinin-producing pathogens and the practical application in agriculture are discussed.

U2 - 10.1104/pp.111.182931

DO - 10.1104/pp.111.182931

M3 - Journal article

C2 - 21813654

SN - 0032-0889

VL - 157

SP - 815

EP - 830

JO - Plant Physiology

JF - Plant Physiology

IS - 2

ER -

Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling

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