Bacterial volatile organic compounds (VOCs) promote growth and induce metabolic changes in rice

Abstract

Plant growth-promoting bacteria (PGPB) represent an eco-friendly alternative to reduce the use of chemical products while increasing the productivity of economically important crops. The emission of small gaseous signaling molecules from PGPB named volatile organic compounds (VOCs) has emerged as a promising biotechnological tool to promote biomass accumulation in model plants (especially Arabidopsis thaliana) and a few crops, such as tomato, lettuce, and cucumber. Rice (Oryza sativa) is the most essential food crop for more than half of the world’s population. However, the use of VOCs to improve this crop performance has not yet been investigated. Here, we evaluated the composition and effects of bacterial VOCs on the growth and metabolism of rice. First, we selected bacterial isolates (IAT P4F9 and E.1b) that increased rice dry shoot biomass by up to 83% in co-cultivation assays performed with different durations of time (7 and 12 days). Metabolic profiles of the plants co-cultivated with these isolates and controls (without bacteria and non-promoter bacteria—1003-S-C1) were investigated via1H nuclear magnetic resonance. The analysis identified metabolites (e.g., amino acids, sugars, and others) with differential abundance between treatments that might play a role in metabolic pathways, such as protein synthesis, signaling, photosynthesis, energy metabolism, and nitrogen assimilation, involved in rice growth promotion. Interestingly, VOCs from IAT P4F9 displayed a more consistent promotion activity and were also able to increase rice dry shoot biomass in vivo. Molecular identification by sequencing the 16S rRNA gene of the isolates IAT P4F9 and E.1b showed a higher identity with Serratia and Achromobacter species, respectively. Lastly, volatilomes of these and two other non-promoter bacteria (1003-S-C1 and Escherichia coli DH5α) were evaluated through headspace solid-phase microextraction coupled with gas chromatography–mass spectrometry. Compounds belonging to different chemical classes, such as benzenoids, ketones, alcohols, sulfide, alkanes, and pyrazines, were identified. One of these VOCs, nonan-2-one, was validated in vitro as a bioactive compound capable of promoting rice growth. Although further analyses are necessary to properly elucidate the molecular mechanisms, our results suggest that these two bacterial isolates are potential candidates as sources for bioproducts, contributing to a more sustainable agriculture.

Bacterial volatile organic compounds from Bacillus zanthoxyli HS-1 enhance tolerance responses against salt and high temperature in cucumber and cabbage

“…As aforementioned, Bacillus spp. could often produce bVOCs that may act as external signals among intra-, inter-species, and even inter-kingdoms (14,32). To examine if the increased tolerance response by the BzaHS1 strain was due to bVOCs released from the strain, we designed a stacked magenta box system to spatially isolate roots from the BzaHS1 strain (Fig.…”

“…Many previous studies illustrate the role of PGPR, including Bacillus spp., Pseudomonas spp., and Rhizobium spp., in regulating abiotic stress tolerance, as well as induced resistance, through direct and indirect mechanisms (11,12,14,15,16,41). Our previous study proposed that exogenous treatment of the BzaHS1 strain might activate IST to protect plants from high salinity stress (26).…”

“…Moreover, this inoculation strategy effectively mitigated the morphological imbalances induced by chemical fertilizers (13). Bacterial volatile organic compounds (bVOCs) are low molecular weight products synthesized and released by PGPR (14). These bVOCs play important roles in plant-microbe interactions and positively affect plant growth and tolerance response to abiotic stresses, such as drought, salinity, and mineral de ciency (15,16).…”

Impact of bacterial volatiles on the plant growth attributes and defense mechanism of rice seedling

“…Ryu et al (2003) [ 41 ], first reported the positive impact caused by bacterial volatiles promoting the growth of Arabidopsis, since then very few research was conducted on the growth promotion of rice by the action of bacterial volatiles [ 10 ]. In our experimental setup, six isolates were used to see if their volatiles could promote rice growth when grown on two petri plates with only airborne signals being transferred between the bacteria and the plants.…”

“…From literature approximately 2000 VOCs have been identified which were emitted by a bacteria and fungi and were discovered on a limited number of microorganisms. BVCs are categorized in alcohols, alkenes, ketones, tepenoids, and other chemical classes [ [8] , [9] , [10] ].…”