Marcelo Pedrosa Gomes

Alteration of plant physiology by glyphosate and its by-product aminomethylphosphonic acid: an overview

It is generally claimed that glyphosate kills undesired plants by affecting the 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) enzyme, disturbing the shikimate pathway. However, the mechanisms leading to plant death may also be related to secondary or indirect effects of glyphosate on plant physiology. Moreover, some plants can metabolize glyphosate to aminomethylphosphonic acid (AMPA) or be exposed to AMPA from different environmental matrices. AMPA is a recognized phytotoxin, and its co-occurrence with glyphosate could modify the effects of glyphosate on plant physiology. The present review provides an overall picture of alterations of plant physiology caused by environmental exposure to glyphosate and its metabolite AMPA, and summarizes their effects on several physiological processes. It particularly focuses on photosynthesis, from photochemical events to C assimilation and translocation, as well as oxidative stress. The effects of glyphosate and AMPA on several plant physiological processes have been linked, with the aim of better understanding their phytotoxicity and glyphosate herbicidal effects.

Reactive oxygen species and seed germination

Reactive oxygen species (ROS) are continuously produced by the metabolically active cells of seeds, and apparently play important roles in biological processes such as germination and dormancy. Germination and ROS accumulation appear to be linked, and seed germination success may be closely associated with internal ROS contents and the activities of ROS-scavenging systems. Although ROS were long considered hazardous molecules, their functions as cell signaling compounds are now well established and widely studied in plants. In seeds, ROS have important roles in endosperm weakening, the mobilization of seed reserves, protection against pathogens, and programmed cell death. ROS may also function as messengers or transmitters of environmental cues during seed germination. Little is currently known, however, about ROS biochemistry or their functions or the signaling pathways during these processes, which are to be considered in the present review.

Ecophysiological and anatomical changes due to uptake and accumulation of heavy metal in Brachiaria decumbens

The growth and developmental characteristics of grasses and their high biodiversity make such plants suitable for remediation of areas contaminated by heavy metals. Nevertheless, heavy metal toxic effect on the plants may cause alteration in their metabolic pathways, such as photosynthesis, respiration, and growth, modifying plant anatomy. This work aimed to evaluate the effect of levels of soil contamination (0, 7.5 % and 15 % m3 m-3) on biomass production, on photosynthetic characteristics and on anatomical changes in roots and leaves of brachiaria (Brachiaria decumbens Stapf.). After seeds were planted, seedlings were uprooted and replanted in vases containing soil at different contamination levels, being left to rest for 120 days. At the end of that time, plants presented reduced yield of root and shoot dry matter, contents of chlorophyll a, chlorophyll b, total chlorophyll and potential photosynthesis with increased of soil contamination. The cell layers of endodermis and exodermis in the root tissues and the cell walls of the xylem and cortical parenchyma all thickened as contamination increased. In the leaf tissues, the adaxial and abaxial epidermis presented increased thickness while the leaf blade presented reduced thickness as contamination increased with consequent change in the root growth rate. In general, the effects of heavy metal increased with the metal concentration. Some results indicate that B. decumbens seems to have some degree of heavy metal tolerance.

Differential effects of glyphosate and aminomethylphosphonic acid (AMPA) on photosynthesis and chlorophyll metabolism in willow plants

We used a willow species (Salix miyabeana cultivar SX64) to examine the differential secondary-effects of glyphosate and aminomethylphosphonic acid (AMPA), the principal glyphosate by-product, on chlorophyll metabolism and photosynthesis. Willow plants were treated with different concentrations of glyphosate (equivalent to 0, 1.4, 2.1 and 2.8kgha(-1)) and AMPA (equivalent to 0, 0.28, 1.4 and 2.8kgha(-1)) and evaluations of pigment contents, chlorophyll fluorescence, and oxidative stress markers (hydrogen peroxide content and antioxidant enzyme activities) in leaves were performed after 12h of exposure. We observed that AMPA and glyphosate trigger different mechanisms leading to decreases in chlorophyll content and photosynthesis rates in willow plants. Both chemicals induced ROS accumulation in willow leaves although only glyphosate-induced oxidative damage through lipid peroxidation. By disturbing chlorophyll biosynthesis, AMPA induced decreases in chlorophyll contents, with consequent effects on photosynthesis. With glyphosate, ROS increases were higher than the ROS-sensitive threshold, provoking chlorophyll degradation (as seen by pheophytin accumulation) and invariable decreases in photosynthesis. Peroxide accumulation in both AMPA and glyphosate-treated plants was due to the inhibition of antioxidant enzyme activities. The different effects of glyphosate on chlorophyll contents and photosynthesis as described in the literature may be due to various glyphosate:AMPA ratios in those plants.

Phosphorous and sulfur nutrition modulate antioxidant defenses in Myracrodruom urundeuva plants exposed to arsenic.

We investigated if plant nutrition and antioxidant system activation are correlated features of arsenic (As)-tolerance in Myracrodruom urundeuva. Plants were grown for 120 days in substrates with 0, 10, 50 and 100mg Askg(-1) and its As-tolerance was demonstrated. As-concentrations greater than 10mgkg(-1) decreased plant growth and photosynthesis but did not induce plant death. Plants coupled alterations in stomatal conductance and transpiration to avoid As-deleterious effects to the photosynthetic apparatus. As-toxicity in M. urundeuva was due to lipid peroxidation induced by hydrogen peroxide accumulation. Ascorbate peroxidase (APX) and gluthatione peroxidase (GPX) had central roles in hydrogen peroxide (H2O2) scavenging in leaves, and their activities were linked to changes in redox potentials (ascorbate and glutathione pools). APX and GPX inactivation/degeneration led to H2O2 accumulation and related lipid peroxidation. Increased phosphorus (P) and sulfur (S) concentrations in leaves were related to increased APX and GPX activities by stimulating increases in glutathione biosynthesis. We concluded that P and S nutrition were directly linked to As-tolerance in M. urundeuva plants by increasing antioxidant system activities.

Phosphorus improves arsenic phytoremediation by Anadenanthera peregrina by alleviating induced oxidative stress.

Due to similarities in their chemical behaviors, studies examining interactions between arsenic (As)—in special arsenate—and phosphorus (P) are important for better understanding arsenate uptake, toxicity, and accumulation in plants. We evaluated the effects of phosphate addition on plant biomass and on arsenate and phosphate uptake by Anadenanthera peregrina, an important Brazilian savanna legume. Plants were grown for 35 days in substrates that received combinations of 0, 10, 50, and 100 mg kg−1 arsenate and 0, 200, and 400 mg kg−1 phosphate. The addition of P increased the arsenic-phytoremediation capacity of A. peregrina by increasing As accumulation, while also alleviating As-induced oxidative stress. Arsenate phytotoxicity in A. peregrina is due to lipid peroxidation, but not hydrogen peroxide accumulation. Added P also increased the activity of important reactive oxygen species-scavenging enzymes (catalase and ascorbate peroxidase) that help prevent lipid peroxidation in leaves. Our findings suggest that applying P represents a feasible strategy for more efficient As phytoremediation using A. peregrina.

Anatomical characteristics and nutrient uptake and distribution associated with the Cd-phytoremediation capacity of Eucalyptus camaldulenses Dehnh

Cadmium (Cd) is a hazardous heavy metal whose concentrations have been increasing in Brazilian soils, largely due to mining activities. Eucalyptus species are widely planted in Brazil to produce raw materials, and the confirmation of their phytoreme diation potential would link their economic and environmental roles. We examined the Cd-tolerance of Eucaliptus camaldulenses Dehnh and the anatomical and physiological features associated with that capacity. Plants were grown under greenhouse conditions in nutrient solutions with increasing concentrations of Cd (0, 15, 25, 45, 90 μmol m -3 ). Shoot biomass production was less sensitive to the phytotoxic effects of cadmium than root biomass production due to low Cd transport rates from roots to shoots. Increases in epidermal and endodermal thickness, changes in the vascular conductive elements of the roots, as well as differential nutrient distributions between roots and shoots are features of Cd tolerance in this species. The Cd tolerance of E. camaldulenses and its high biomass production support its potential use in Cd phytoremediation programs.

Cadmium effects on mineral nutrition of the Cd-hyperaccumulator Pfaffia glomerata

A plant’s ability to survive in a stressful environment is correlated with its nutritional status, which can be affected by cadmium (Cd) uptake. The present study evaluated the influence of Cd on the concentrations and distributions of nutrients in the roots and shoots of the Cd-hyperaccumulator Pfaffia glomerata (Sprengel) Pedersen. Plantlets were cultivated in nutrient solutions containing increasing Cd concentrations during 20 days under greenhouse conditions, and the concentrations of Cd and essential macro- (N, P, K, Ca, Mg and S) and micro- (Zn, Fe, Mn, Cu) elements in the roots and shoots were subsequently determined. Cd did not affect the plant biomass production. Cd accumulation was found to be higher in roots than in shoots, and influenced the distribution of macro and micro elements in those plants. Despite the high phytotoxicity of this element, our results indicated the existence of Cd-tolerance mechanisms in both nutrient uptake and distribution processes that enabled these plants to survive in Cd-contaminated sites.

Impact of phosphate on glyphosate uptake and toxicity in willow

Phosphate (PO4(3-)) has been shown to increase glyphosate uptake by willow, a plant species known for its phytoremediation potential. However, it remains unclear if this stimulation of glyphosate uptake can result in an elevated glyphosate toxicity to plants (which could prevent the use of willows in glyphosate-remediation programs). Consequently, we studied the effects of PO4(3-) on glyphosate uptake and toxicity in a fast growing willow cultivar (Salix miyabeana SX64). Plants were grown in hydroponic solution with a combination of glyphosate (0, 0.001, 0.065 and 1 mg l(-1)) and PO4(3-) (0, 200 and 400 mg l(-1)). We demonstrated that PO4(3-) fertilization greatly increased glyphosate uptake by roots and its translocation to leaves, which resulted in increased shikimate concentration in leaves. In addition to its deleterious effects in photosynthesis, glyphosate induced oxidative stress through hydrogen peroxide accumulation. Although it has increased glyphosate accumulation, PO4(3-) fertilization attenuated the herbicides deleterious effects by increasing the activity of antioxidant systems and alleviating glyphosate-induced oxidative stress. Our results indicate that in addition to the glyphosate uptake, PO4(3-) is involved in glyphosate toxicity in willow by preventing glyphosate induced oxidative stress.

Consequences of phosphate application on glyphosate uptake by roots: Impacts for environmental management practices.

Phosphate (PO4(3-)) fertilization is a common practice in agricultural fields also targets for glyphosate application. Due to their chemical similarities, PO4(3-) and glyphosate compete for soil adsorbing sites, with PO4(3-) fertilization increasing glyphosate bioavailability in the soil solution. After PO4(3-) fertilization, its concentration will be elevated in the soil solution and both PO4(3-) and glyphosate will be readily available for runoff into aquatic ecosystems. In this context, man-made riparian buffer strips (RBS) at the interface of agricultural lands and waterways can be used as a green technology to mitigate water contamination. The plants used in RBS form a barrier to agricultural wastes that can limit runoff, and the ability of these plants to take up these compounds through their roots plays an important role in RBS efficacy. However, the implications of PO4(3-) for glyphosate uptake by roots are not yet clearly demonstrated. Here, we addressed this problem by hydroponically cultivating willow plants in nutrient solutions amended with glyphosate and different concentrations of PO4(3-), assuring full availability of both chemicals to the roots. Using a phosphate carrier inhibitor (phosphonophormic acid-PFA), we found that part of the glyphosate uptake is mediated by PO4(3-) transporters. We observed, however, that PO4(3-) increased glyphosate uptake by roots, an effect that was related to increased root cell membrane stability. Our results indicate that PO4(3-) has an important role in glyphosate physiological effects. Under agricultural conditions, PO4(3-) fertilization can amplify glyphosate efficiency by increasing its uptake by the roots of undesired plants. On the other hand, since simultaneous phosphate and glyphosate runoffs are common, non-target species found near agricultural fields can be affected.