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Stereoisomers of the Bacterial Volatile Compound 2,3-Butanediol Differently Elicit Systemic Defense Responses of Pepper against Multiple Viruses in the Field.

ABSTRACT: The volatile compound 2,3-butanediol, which is produced by certain strains of root-associated bacteria, consists of three stereoisomers, namely, two enantiomers (2R,3R- and 2S,3S-butanediol) and one meso compound (2R,3S-butanediol). The ability of 2,3-butanediol to induce plant resistance against pathogenic fungi and bacteria has been investigated; however, little is known about its effects on induced resistance against viruses in plants. To investigate the effects of 2,3-butanediol on plant systemic defense against viruses, we evaluated the disease control capacity of each of its three stereoisomers in pepper. Specifically, we investigated the optimal concentration of 2,3-butanediol to use for disease control against Cucumber mosaic virus and Tobacco mosaic virus in the greenhouse and examined the effects of drench application of these compounds in the field. In the field trial, treatment with 2R,3R-butanediol and 2R,3S-butanediol significantly reduced the incidence of naturally occurring viruses compared with 2S,3S-butanediol and control treatments. In addition, 2R,3R-butanediol treatment induced the expression of plant defense marker genes in the salicylic acid, jasmonic acid, and ethylene signaling pathways to levels similar to those of the benzothiadiazole-treated positive control. This study reports the first field trial showing that specific stereoisomers of 2,3-butanediol trigger plant immunity against multiple viruses.

SUBMITTER: Kong HG

PROVIDER: S-EPMC5829544 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Stereoisomers of the Bacterial Volatile Compound 2,3-Butanediol Differently Elicit Systemic Defense Responses of Pepper against Multiple Viruses in the Field.

Kong Hyun G HG Shin Teak S TS Kim Tae H TH Ryu Choong-Min CM

Frontiers in plant science 20180222

The volatile compound 2,3-butanediol, which is produced by certain strains of root-associated bacteria, consists of three stereoisomers, namely, two enantiomers (2R,3R- and 2S,3S-butanediol) and one meso compound (2R,3S-butanediol). The ability of 2,3-butanediol to induce plant resistance against pathogenic fungi and bacteria has been investigated; however, little is known about its effects on induced resistance against viruses in plants. To investigate the effects of 2,3-butanediol on plant sys ...[more]

PMID: 29527214

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Project description:Volatile compounds, such as short chain alcohols, acetoin, and 2,3-butanediol, produced by certain strains of root-associated bacteria (rhizobacteria) elicit induced systemic resistance in plants. The effects of bacterial volatile compounds (BVCs) on plant and fungal growth have been extensively studied; however, the impact of bacterial BVCs on bacterial growth remains poorly understood. In this study the effects of a well-characterized bacterial volatile, 2,3-butanediol, produced by the rhizobacterium Bacillus subtilis, were examined in the rhizosphere. The nature of 2,3-butanediol on bacterial cells was assessed, and the effect of the molecule on root colonization was also determined. Pepper roots were inoculated with three B. subtilis strains: the wild type, a 2,3-butanediol overexpressor, and a 2,3-butanediol null mutant. The B. subtilis null strain was the first to be eliminated in the rhizosphere, followed by the wild-type strain. The overexpressor mutant was maintained at roots for the duration of the experiment. Rhizosphere colonization by a saprophytic fungus declined from 14 days post-inoculation in roots treated with the B. subtilis overexpressor strain. Next, exudates from roots exposed to 2,3-butanediol were assessed for their impact on fungal and bacterial growth in vitro. Exudates from plant roots pre-treated with the 2,3-butanediol overexpressor were used to challenge various microorganisms. Growth was inhibited in a saprophytic fungus (Trichoderma sp.), the 2,3-butanediol null B. subtilis strain, and a soil-borne pathogen, Ralstonia solanacearum. Direct application of 2,3-butanediol to pepper roots, followed by exposure to R. solanacearum, induced expression of Pathogenesis-Related (PR) genes such as CaPR2, CaSAR8.2, and CaPAL. These results indicate that 2,3-butanediol triggers the secretion of root exudates that modulate soil fungi and rhizosphere bacteria. These data broaden our knowledge regarding bacterial volatiles in the rhizosphere and their roles in bacterial fitness and as important inducers of plant defenses.

Project description:BackgroundPreviously, a safe strain, Bacillus amyloliquefaciens B10-127 was identified as an excellent candidate for industrial-scale microbial fermentation of 2,3-butanediol (2,3-BD). However, B. amyloliquefaciens fermentation yields large quantities of acetoin, lactate and succinate as by-products, and the 2,3-BD yield remains prohibitively low for commercial production.Methodology/principal findingsIn the 2,3-butanediol metabolic pathway, glyceraldehyde-3-phosphate dehydrogenase (GAPDH) catalyzes the conversion of 3-phosphate glyceraldehyde to 1,3-bisphosphoglycerate, with concomitant reduction of NAD(+) to NADH. In the same pathway, 2,3-BD dehydrogenase (BDH) catalyzes the conversion of acetoin to 2,3-BD with concomitant oxidation of NADH to NAD(+). In this study, to improve 2,3-BD production, we first over-produced NAD(+)-dependent GAPDH and NADH-dependent BDH in B. amyloliquefaciens. Excess GAPDH reduced the fermentation time, increased the 2,3-BD yield by 12.7%, and decreased the acetoin titer by 44.3%. However, the process also enhanced lactate and succinate production. Excess BDH increased the 2,3-BD yield by 16.6% while decreasing acetoin, lactate and succinate production, but prolonged the fermentation time. When BDH and GAPDH were co-overproduced in B. amyloliquefaciens, the fermentation time was reduced. Furthermore, in the NADH-dependent pathways, the molar yield of 2,3-BD was increased by 22.7%, while those of acetoin, lactate and succinate were reduced by 80.8%, 33.3% and 39.5%, relative to the parent strain. In fed-batch fermentations, the 2,3-BD concentration was maximized at 132.9 g/l after 45 h, with a productivity of 2.95 g/l·h.Conclusions/significanceCo-overexpression of bdh and gapA genes proved an effective method for enhancing 2,3-BD production and inhibiting the accumulation of unwanted by-products (acetoin, lactate and succinate). To our knowledge, we have attained the highest 2,3-BD fermentation yield thus far reported for safe microorganisms.

Dataset Information

Stereoisomers of the Bacterial Volatile Compound 2,3-Butanediol Differently Elicit Systemic Defense Responses of Pepper against Multiple Viruses in the Field.

Publications

Stereoisomers of the Bacterial Volatile Compound 2,3-Butanediol Differently Elicit Systemic Defense Responses of Pepper against Multiple Viruses in the Field.

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