Rhizobacterium‐derived diacetyl modulates plant immunity in a phosphate‐dependent manner

Abstract

Plants establish mutualistic associations with beneficial microbes while deploying the immune system to defend against pathogenic ones. Little is known about the interplay between mutualism and immunity and the mediator molecules enabling such crosstalk. Here, we show that plants respond differentially to a volatile bacterial compound through integral modulation of the immune system and the phosphate-starvation response (PSR) system, resulting in either mutualism or immunity. We found that exposure of Arabidopsis thaliana to a known plant growth-promoting rhizobacterium can unexpectedly have either beneficial or deleterious effects to plants. The beneficial-to-deleterious transition is dependent on availability of phosphate to the plants and is mediated by diacetyl, a bacterial volatile compound. Under phosphate-sufficient conditions, diacetyl partially suppresses plant production of reactive oxygen species (ROS) and enhances symbiont colonization without compromising disease resistance. Under phosphate-deficient conditions, diacetyl enhances phytohormone-mediated immunity and consequently causes plant hyper-sensitivity to phosphate deficiency. Therefore, diacetyl affects the type of relation between plant hosts and certain rhizobacteria in a way that depends on the plant's phosphate-starvation response system and phytohormone-mediated immunity.

Latent defense response to non-pathogenic microbial factors impairs plant-rhizobacteria mutualism

“…Because GMVs decrease defense responses in Col-0 plants ( Figure 3F), it is apparent that these microbial products are not considered by wild type plants as pathogen signals. This pattern 20 possibly reflects plant's ability in distinguishing beneficial microbes from pathogens. On the other hand, the transcriptome comparison between gp1-2 and Col-0 highlights a group of 52 defense response genes, which are induced by GMVs only in gp1-2 but not in Col-0 (Dataset S1).…”

“…Subsequently, whole genome sequencing revealed a C-to-T point mutation in the second exon of the gene At2g43710. This point mutation 20 was predicted to cause an amino acid change from Thr155 to Ile ( Figure S2A).…”

“…When exposed to GMVs, SA-treated plants showed less increases in fresh weight compared to plants without SA treatments ( Figure S5A and B), indicating that the activated SA signaling contributes to the suppression of plant inducible vigor in the gp1 mutant. 20 Arabidopsis EDS1 (Enhanced Disease Susceptibility 1) is required for SA production and R gene mediated disease resistance (25). To investigate whether SA-mediated defense signaling is necessary for the suppression of inducible vigor in gp1, we generated an eds1 gp1-1 double mutant ( Figure S5C), and treated the eds1 gp1-1 double mutant with GMVs.…”

“…Previous studies have reported that GB03-produced microbial volatiles (hereafter referred to as GMVs) cause multiple beneficial effects on plants, such as enhanced lateral root development and increased contents of photosynthetic apparatus, through modulation of phytohormone homeostasis and nutrient uptake (17)(18)(19), although it remains 25 unclear how plant biological processes were integrated by the microbial factors to produce the multiple beneficial traits. In addition, a recent study demonstrated that diacetyl, a GMV component, has opposing effects on GB03-plant association under phosphate-sufficient and phosphatedeficient conditions (20). These findings points to the importance to identify plant molecular factors that are indispensable for proper responses to PGPR.…”

“…In addition to these non-volatile compounds, some PGPR strains also release microbial volatiles compounds capable of affecting plant physiology under normal and stressed conditions (11,14) . 20 B. amyloliquefaciens strain GB03 is an established beneficial microbe to plants both in soil and in artificial medium (11,15,16). Previous studies have reported that GB03-produced microbial volatiles (hereafter referred to as GMVs) cause multiple beneficial effects on plants, such as enhanced lateral root development and increased contents of photosynthetic apparatus, through modulation of phytohormone homeostasis and nutrient uptake (17)(18)(19), although it remains 25 unclear how plant biological processes were integrated by the microbial factors to produce the multiple beneficial traits.…”