Increased Glyphosate-Induced Gene Expression in the Shikimate Pathway Is Abolished in the Presence of Aromatic Amino Acids and Mimicked by Shikimate

Abstract

The herbicide glyphosate inhibits the plant enzyme 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) in the aromatic amino acid (AAA) biosynthetic pathway, also known as the shikimate pathway. Amaranthus palmeri is a fast-growing weed, and several populations have evolved resistance to glyphosate through increased EPSPS gene copy number. The main objective of this study was to elucidate the regulation of the shikimate pathway and determine whether the regulatory mechanisms of glyphosate-sensitive and glyphosate-resistant plants were different. Leaf disks of sensitive and resistant (due to EPSPS gene amplification) A. palmeri plants were incubated for 24 h with glyphosate, AAA, glyphosate + AAA, or several intermediates of the pathway: shikimate, quinate, chorismate and anthranilate. In the sensitive population, glyphosate induced shikimate accumulation and induced the gene expression of the shikimate pathway. While AAA alone did not elicit any change, AAA applied with glyphosate abolished the effects of the herbicide on gene expression. It was not possible to fully mimic the effect of glyphosate by incubation with any of the intermediates, but shikimate was the intermediate that induced the highest increase (three-fold) in the expression level of the genes of the shikimate pathway of the sensitive population. These results suggest that, in this population, the lack of end products (AAA) of the shikimate pathway and shikimate accumulation would be the signals inducing gene expression in the AAA pathway after glyphosate application. In general, the effects on gene expression detected after the application of the intermediates were more severe in the sensitive population than in the resistant population. These results suggest that when EPSPS is overexpressed, as in the resistant population, the regulatory mechanisms of the AAA pathway are disrupted or buffered. The mechanisms underlying this behavior remain to be elucidated.

Unravelling the Phytotoxic Effects of Glyphosate on Sensitive and Resistant Amaranthus palmeri Populations by GC–MS and LC–MS Metabolic Profiling

“…By far, the most highly accumulated metabolite after glyphosate is shikimate so that its content is commonly used as an indicator of glyphosate sensitivity [ 27 , 31 , 32 , 33 ]. Moreover, recently it has been demonstrated that several metabolic disturbances elicited after glyphosate treatments are mediated by shikimate accumulation, as glyphosate effects were mimicked in plants supplemented with exogenous shikimate [ 36 ].…”

Hormesis effects in tomato plant growth and photosynthesis due to acephate exposure based on physiology and transcriptomic analysis

“…It has been suggested that low‐dose stress triggers plant tolerance mechanisms, protecting plants against subsequent high‐level environmental stress 9 . Plant adaptive responses are somewhat specific to environmental factors, since these responses are designed to eliminate specific disruptions by stressors 10–13 . However, it remains unclear whether stimulated traits of plant hormesis induced by mild stressors differ, and how non‐specific (due to the need to activate functions relevant to survival and suppress other functions with any stress impacts) and specific (by the nature of the factor and the ‘points’ of its impact on plant metabolism) adaptive mechanisms contribute to hormesis stimulation in plants 14 .…”

“…9 Plant adaptive responses are somewhat specific to environmental factors, since these responses are designed to eliminate specific disruptions by stressors. [10][11][12][13] However, it remains unclear whether stimulated traits of plant hormesis induced by mild stressors differ, and how non-specific (due to the need to activate functions relevant to survival and suppress other functions with any stress impacts) and specific (by the nature of the factor and the 'points' of its impact on plant metabolism) adaptive mechanisms contribute to hormesis stimulation in plants. 14 Understanding how plants adapt to environmental stressors is necessary to provide foundation theories to elicit a consistent response allowing researchers to identify the likely processes leading to greater productivity or stress tolerance, which is important for improving agricultural production and food security.…”

Transcriptome and UPLC-MS/MS reveal mechanisms of amino acid biosynthesis in sweet orange ‘Newhall’ after different rootstocks grafting

“…Several enzymes are involved in amino acid biosynthesis in plants, with each enzyme providing a specific function. For example, the production of aromatic AAs necessary for plant metabolism, such as L-tryptophan and L-phenylalanine, depends on the shikimate pathway ( Zulet-Gonzalez et al., 2020 ; Bergman et al., 2022 ; Kanaris et al., 2022 ). 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase (DAHP) is an important enzyme in controlling carbon entering the shikimate pathway ( Mir et al., 2015 ).…”