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

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.

Role of Cytokinins for Interactions of Plants With Microbial Pathogens and Pest Insects

“…hormones. However, recently the role of cytokinin in inducing immunity in plant upon plant-pathogenic interaction has also been recognised (Grosskinsky et al, 2011;Grosskinsky et al, 2016;Naseem et al, 2014;Spallek et al, 2017;Dowd et al, 2017;Siddique et al, 2015;Shanks et al, 2016).…”

Root symbionts: Powerful drivers of plant above‐ and belowground indirect defenses

“…Other hormones, such as abscisic acid, ethylene, or salicylic acid might also be involved in orchestrating anti-herbivore defenses in roots, but this remains to be fully elucidated (Johnson et al, 2016). What is clear, however, is that soil microbes can influence plant hormonal pathways (e.g., Cameron et al, 2013;de Zelicourt et al, 2013;Großkinsky et al, 2016), therefore likely influencing belowground tritrophic interactions, since induction of root exudates is also controlled by hormonal signaling (Pierre et al, 2012;Johnson et al, 2016). For example, soil fungi of the genus Trichoderma, which are highly abundant in the rhizosphere, produce a wide array of secondary metabolites (Contreras-Cornejo et al, 2016), including plant hormones such as auxins (Contreras-Cornejo et al, 2009), which can change defense induction and plant immunity (Contreras-Cornejo et al, 2016).…”

Potential modes of action of Pseudomonas fluorescens ZX during biocontrol of blue mold decay on postharvest citrus

“…19 As an effective biocontrol agent, P. fluorescens has been studied extensively for its use in preventing plant disease of the rhizosphere. At present, it is generally believed that the main antagonistic mechanisms of P. fluorescens during control of plant pathogens include parasitism, 20,21 competition for nutrients and space, 12,[20][21][22] production of secondary resistance metabolites [23][24][25] and initiation of systemic resistance. [25][26][27] Many studies have shown that the mechanisms of action of biocontrol agents are influenced by many factors, such as the fungal pathogen, plant host and storage environment, and are not associated with only a single mode of action.…”