Bacterial volatiles promote growth in Arabidopsis

Abstract

Several chemical changes in soil are associated with plant growth-promoting rhizobacteria (PGPR). Some bacterial strains directly regulate plant physiology by mimicking synthesis of plant hormones, whereas others increase mineral and nitrogen availability in the soil as a way to augment growth. Identification of bacterial chemical messengers that trigger growth promotion has been limited in part by the understanding of how plants respond to external stimuli. With an increasing appreciation of how volatile organic compounds signal plants and serve in plant defense, investigations into the role of volatile components in plant-bacterial systems now can follow. Here, we present chemical and plant-growth data showing that some PGPR release a blend of volatile components that promote growth of Arabidopsis thaliana. In particular, the volatile components 2,3-butanediol and acetoin were released exclusively from two bacterial strains that trigger the greatest level of growth promotion. Furthermore, pharmacological applications of 2,3-butanediol enhanced plant growth whereas bacterial mutants blocked in 2,3-butanediol and acetoin synthesis were devoid in this growth-promotion capacity. The demonstration that PGPR strains release different volatile blends and that plant growth is stimulated by differences in these volatile blends establishes an additional function for volatile organic compounds as signaling molecules mediating plant-microbe interactions.

Figure 1

Quantification of growth promotion in A. thaliana with exposure to airborne chemicals released from six growth-promoting bacterial strains compared with a nongrowth-promoting E. coli strain DH5α and water treatment alone; representative examples of 10-day-old A. thaliana seedlings grown on I plates with airborne exposure to bacteria strains and water treatment are shown in Inset. The I plates were prepared as gnotobiotic systems so that the inoculated bacteria were the only microorganisms present.

Figure 2

Chromatographic profiles of volatiles from bacteria strains IN937a and GB03, both of which promote growth by the emission of volatile chemicals, compared with a growth-promoting strain that does not trigger promotion by volatile emissions 89B61, a nongrowth-promoting bacterial strain DH5α, and an uninoculated medium control. Compounds positively identified include 3-hydroxy-2-butanone [1], 2,3-butanediol [2], decane [6], tetramethyl pyrazine [9], undecane [10], decanal [13], dodecane [14], 2-undecanone [16], 2-tridecanone [17], and 2-tridecanol [18]; nonyl acetate was added as an internal standard (IS). Asterisks in the lower chromatograms designate compounds that align with numbered peaks above.

Figure 3

Proposed pathways for anaerobic fermentation in B. subtilis (modified from ref. 11). Enzymes with known coding genes include pyruvate dehydrogenase (PDH), lactate dehydrogenase (LDH), pyruvate decarboxylase (PDC), alcohol dehydrogenase (ADH), acetolactate synthase (ALSS), acetolactate decarboxylase (ALSD), and acetoin reductase (AR).

Figure 4

Growth promotion of A. thaliana ecotype Col-0 with exposure to extracted bacterial volatiles from growth-promoting (GB03 and IN937a) and nongrowth-promoting (DH5α) bacteria and synthetic 2,3-butanediol (A) and exposure to volatiles released from B. subtilis WT (168) and mutant strains defective in the production of 2,3-butanediol (BSIP1173 and BSIP1174) (B). Different letters indicate significant differences between treatments according to least significant difference at P = 0.05.