Hormesis of glyphosate on ferulic acid metabolism and antifungal volatile production in rice root biocontrol endophyte Burkholderia cepacia LS-044

Abstract

Glyphosate (GP, N-phosphonomethyl glycine) is one of the most popular organophosphate herbicides widely used in agricultural practices worldwide. There have been extensive reports on the biohazard attributes and hormetic impacts of GP on plant and animal systems. However, the effects of GP on plant growth-promoting microbes and its ecological relevance remain unknown. Here, we show that GP does exert a hormetic impact on Burkholderia cepacia LS-044, a rice (Oryza sativa ssp. japonica cv. Tainung 71) root endophytic isolate. We used increasing doses of ferulic acid (FA, 1-25 mM) and GP (0.5-5 mM) to test the growth and antifungal volatile production in LS-044 by electrochemical, liquid chromatographic, gas chromatographic and spectrophotometric means. GP treatment at a low dose (0.5 mM) increased FA utilization and significantly (P < 0.0001) enhanced antifungal volatile activity in LS-044. Although FA (1 mM) was rapidly utilized by LS-044, no chromatographically detectable utilization of GP was observed at tested doses (0.5-5 mM). LS-044 emitted predominant amounts of tropone in addition to moderate-to-minor amounts of diverse ketones and/or their derivatives (acetone, acetophenone, 2-butanone, 1-propanone, 1-(2-furanyl-ethanone, 1-phenyl-1-propanone and 1-(3-pyridinyl)-1-propanone), d-menthol, 2-methoxy-3-(1-methylethyl)-pyrazine, dimethyl disulfide, pyridine and ammonium carbamate when grown under GP supplement. GP hormesis on LS-044 induced phenotypic variations in O. sativa ssp. japonica cv. Tainan 11 as evident through seed germination assay. Genes involved in the transformation of FA, and a key gene encoding 5-enolpyruvylshikimate 3-phosphate synthase (EPSPS) with Gly-94 and Tyr-95 residues localized at active site most likely rendering EPSPS sensitivity to GP, were detected in LS-044. This is the first report on the GP hormesis influencing morphological and metabolic aspects including volatile emission in a biocontrol bacterium that could modulate rice plant phenotype.

Keywords: Allelochemical; Antifungal volatiles; Autotoxicity; Burkholderia cepacia complex; Herbicide; Hormesis; Roundup.