Arsenic hyperaccumulation induces metabolic reprogramming in Pityrogramma calomelanos to reduce oxidative stress

Abstract

Arsenic (As) pollution is a major environmental concern due to its worldwide distribution and high toxicity to organisms. The fern Pityrogramma calomelanos is one of the few plant species known to be able to hyperaccumulate As, although the mechanisms involved are largely unknown. This study aimed to investigate the metabolic adjustments involved in the As-tolerance of P. calomelanos. For this purpose, ferns with five to seven fronds were exposed to a series of As concentrations. Young fronds were used for biochemical analysis and metabolite profiling using gas chromatography-mass spectrometry. As treatment increased the total concentration of proteins and soluble phenols, enhanced peroxidase activities, and promoted disturbances in nitrogen and carbon metabolism. The reduction of the glucose pool was one of the striking responses to As. Remarkable changes in amino acids levels were observed in As-treated plants, including those related to biosynthesis of glutathione and phenols, osmoregulation and two photorespiratory intermediates. In addition, increases in polyamines levels and antioxidant enzyme activities were observed. In summary, this study indicates that P. calomelanos tolerates high concentration of As due to its capacity to upregulate biosynthesis of amino acids and antioxidants, without greatly disturbing central carbon metabolism. At extremely high As concentrations, however, this protective mechanism fails to block reactive oxygen species production, leading to lipid peroxidation and leaf necrosis.

Effect of arsenic stress on 5-methylcytosine, photosynthetic parameters and nutrient content in arsenic hyperaccumulator Pteris cretica (L.) var. Albo-lineata

“…The primary detoxification of As in the cells of terrestrial plants relies on rapid reduction of As V to As III and the formation of As III -glutathione or As III -phytochelatin complexes, which are eventually transported to the vacuole. Disturbances in cellular processes, caused by a toxic excess of As, induce oxidative stress responses [15][16][17], methylation of both As forms in P. cretica [18], and epigenetic changes in DNA [19]. In this study, we aimed to gain insight into the context of As hyperaccumulation and plant senescence in Pteris cretica var.…”

Multi-Component Antioxidative System and Robust Carbohydrate Status, the Essence of Plant Arsenic Tolerance

“…Unfortunately, the As effect on carbohydrate status needs further clarification, as not many of the studies devoted to the As influence on saccharide metabolism used various plant species, a diverse experimental design, or material of different plant ages; moreover, these studies led to contradictory results (decreased/increased or even fluctuating saccharide levels, e.g., in rice [35], bean [36], wheat [37], potato [18], or tomato [16]. Importantly, As-tolerant fern Pityrogramma calomelanos exhibited relative stable carbohydrate levels upon arsenic stress [38].…”

The contents of free amino acids and elements in As-hyperaccumulator Pteris cretica and non-hyperaccumulator Pteris straminea during reversible senescence

“…High levels of Gly and its negative correlation with Ser were only found in PS. Their biosynthesis pathways are linked (Nunes-Nesi et al 2008, Campos et al 2016) and they are also products of significant metabolites connected with reversible senescence (accumulated Ser initiates a senescence; Zhu et al Vol. 63, 2017, No.…”

“…), cytokinins and mainly for substituted As III/V species with CH 3 . The profiling AA content in Pteris is unknown, although the AA content is significantly affected by As content in hyperaccumulating ferns Pityrogramma calomelanos (Campos et al 2016). To determine the non-stress metabolism of AAs in plants it is necessary to define reversible senescence in the Pteris genus.…”