Metabolite profiles across populations of Palmer amaranth (Amaranthus palmeri) highlight the specificity and inducibility of phytochemical response to glyphosate stress

Abstract

SUMMARYModifications of the phytochemical profile form a vital component of physiological stress adaptation in plants. However, the specificity and uniqueness of phytochemical changes with respect to the identity of stressors is less known. Here, we investigated the commonality and specificity of metabolic perturbations induced by a specific stressor – glyphosate, and a general stressor – drought, across multiple glyphosate-resistant (GR) and -susceptible (GS) biotypes of a dominant agricultural weed, Amaranthus palmeri. In the absence of stress, the native metabolite profile of GS- and GR-biotypes was similar, and amplification of the EPSPS gene in GR-biotypes did not translate to a higher abundance of downstream metabolites. Further, glyphosate treatment initially inhibited the shikimate pathway in both GS- and GR-biotypes, from which the GR-biotypes recovered, indicating inducibility in the functionalization of the EPSPS enzyme. The accumulation of phenylpropanoids produced downstream of the shikimate pathway, was higher in GR-biotypes than GS-biotypes, with a preferential accumulation of compounds with higher antioxidant potential. However, this increase was not observed in response to drought treatment, where the metabolic perturbations were pervasive but limited in magnitude compared to glyphosate stress. Overall, while native phytochemistry of A. palmeri was similar irrespective of the level of glyphosate susceptibility, the specific stressor, glyphosate, imparted metabolic perturbations that were localized but higher in magnitude, while the specificity of phytochemical response to the general stressor, drought, was minimal. Taken together, these results suggest that, at the metabolic level, the glyphosate resistance mechanism in A. palmeri is partly induced and specific to herbicide stress.SIGNIFICANCE STATEMENTUnderstanding changes in physiology, especially those related to secondary metabolites with adaptogenic functions, is imperative to decipher the basis of stress adaptation in plants. This study provides critical information on native and stress-induced phytochemical differences between multiple glyphosate-resistant and -susceptible weed biotypes, thus, shedding light on the metabolome-level orchestration of gene amplification-mediated glyphosate resistance mechanism in an economically devastating weed, Palmer amaranth (Amaranthus palmeri).