Effects of Combined Low Glutathione with Mild Oxidative and Low Phosphorus Stress on the Metabolism of Arabidopsis thaliana

Abstract

Plants possess highly sensitive mechanisms that monitor environmental stress levels for a dose-dependent fine-tuning of their growth and development. Differences in plant responses to severe and mild abiotic stresses have been recognized. Although many studies have revealed that glutathione can contribute to plant tolerance to various environmental stresses, little is known about the relationship between glutathione and mild abiotic stress, especially the effect of stress-induced altered glutathione levels on the metabolism. Here, we applied a systems biology approach to identify key pathways involved in the gene-to-metabolite networks perturbed by low glutathione content under mild abiotic stress in Arabidopsis thaliana. We used glutathione synthesis mutants (cad2-1 and pad2-1) and plants overexpressing the gene encoding γ-glutamylcysteine synthetase, the first enzyme of the glutathione biosynthetic pathway. The plants were exposed to two mild stress conditions—oxidative stress elicited by methyl viologen and stress induced by the limited availability of phosphate. We observed that the mutants and transgenic plants showed similar shoot growth as that of the wild-type plants under mild abiotic stress. We then selected the synthesis mutants and performed multi-platform metabolomics and microarray experiments to evaluate the possible effects on the overall metabolome and the transcriptome. As a common oxidative stress response, several flavonoids that we assessed showed overaccumulation, whereas the mild phosphate stress resulted in increased levels of specific kaempferol- and quercetin-glycosides. Remarkably, in addition to a significant increased level of sugar, osmolytes, and lipids as mild oxidative stress-responsive metabolites, short-chain aliphatic glucosinolates over-accumulated in the mutants, whereas the level of long-chain aliphatic glucosinolates and specific lipids decreased. Coordinated gene expressions related to glucosinolate and flavonoid biosynthesis also supported the metabolite responses in the pad2-1 mutant. Our results suggest that glutathione synthesis mutants accelerate transcriptional regulatory networks to control the biosynthetic pathways involved in glutathione-independent scavenging metabolites, and that they might reconfigure the metabolic networks in primary and secondary metabolism, including lipids, glucosinolates, and flavonoids. This work provides a basis for the elucidation of the molecular mechanisms involved in the metabolic and transcriptional regulatory networks in response to combined low glutathione content with mild oxidative and nutrient stress in A. thaliana.

Silicon Compensates Phosphorus Deficit-Induced Growth Inhibition by Improving Photosynthetic Capacity, Antioxidant Potential, and Nutrient Homeostasis in Tomato

“…Phosphorus is an essential macronutrient for plant growth and development, but its deficiency in most soils has been a major handicap for sustainable crop production worldwide [4]. In addition to the use of chemical fertilizers, a number of other approaches have been suggested to mitigate P deficiency-induced hazards in plants [2,3,5,37,38]. In particular, the applications of exogenous growth regulators/elements as a means for agronomic management have shown promising results in nutrient-deficit soils.…”

“…Phosphorus is an essential macroelement that not only stimulates plant growth but also affects plant responses due to its direct involvement in energy production (ATP) and signaling cascades by mediating phosphorylation of various proteins [4,6,38]. Thus, P deficiency impairs nutrient homeostasis, leading to massive physiological and metabolic changes in plants [37,46]. Despite a large number of studies in Si-mediated tolerance to abiotic stresses, the underlying mechanisms remain largely unknown [12].…”

Metabolic Reprogramming in Leaf Lettuce Grown Under Different Light Quality and Intensity Conditions Using Narrow-Band LEDs

“…Jung and colleagues have previously reported a significant correlation between metabolites detected using GC–MS and LC–MS and their antioxidant activity in rice leaves grown under different light conditions using LEDs 45 . Our systems biology approach previously assessed comprehensive metabolic and transcriptional reprogramming of Arabidopsis to UV-B light 46 and characterised metabolic effects of combined low glutathione with mild oxidative and low phosphorus stress in Arabidopsis 47 . These results suggest that the combination of different light regimes with or without mild stresses intensifies specific metabolic pathways involved in the production of antioxidants.…”

Comparing normalization methods and the impact of noise

“…Thus, even subtle changes in metabolite concentrations may provide important insights into disease progression, (Cuykx, Claes, Rodrigues, Vanhaecke, Covaci 2018) drug resistance, (Thulin, Thulin, Andersson 2017) or a response to numerous stress factors ( e.g., environmental toxins, nutrient limitation, genetic mutation, etc. )(Doran, Knee, Wang, Rzezniczak, Parkes, Li, Merritt 2017; Fukushima, Iwasa, Nakabayashi, Kobayashi, Nishizawa, Okazaki, Saito et al 2017; Jung, Lee, Seo, Hwang 2017). Unfortunately, like genomics and proteomics, these metabolite differences are easily obscured by the natural variance that occurs between biological replicates or by inconsistencies in sample sizes.…”

“…A variety of procedures are currently available to normalize NMR metabolomics data (Fukushima, Iwasa, Nakabayashi, Kobayashi, Nishizawa, Okazaki, Saito et al 2017; Hochrein, Zacharias, Taruttis, Samol, Engelmann, Spang, Oefner et al 2015). Since each algorithm addresses systematic variations in a different manner, the correct choice of a normalization scheme can be challenging.…”