Fernanda S. Farnese

When Bad Guys Become Good Ones: The Key Role of Reactive Oxygen Species and Nitric Oxide in the Plant Responses to Abiotic Stress

The natural environment of plants is composed of a complex set of abiotic stresses and their ability to respond to these stresses is highly flexible and finely balanced through the interaction between signaling molecules. In this review, we highlight the integrated action between reactive oxygen species (ROS) and reactive nitrogen species (RNS), particularly nitric oxide (NO), involved in the acclimation to different abiotic stresses. Under stressful conditions, the biosynthesis transport and the metabolism of ROS and NO influence plant response mechanisms. The enzymes involved in ROS and NO synthesis and scavenging can be found in different cells compartments and their temporal and spatial locations are determinant for signaling mechanisms. Both ROS and NO are involved in long distances signaling (ROS wave and GSNO transport), promoting an acquired systemic acclimation to abiotic stresses. The mechanisms of abiotic stresses response triggered by ROS and NO involve some general steps, as the enhancement of antioxidant systems, but also stress-specific mechanisms, according to the stress type (drought, hypoxia, heavy metals, etc.), and demand the interaction with other signaling molecules, such as MAPK, plant hormones, and calcium. The transduction of ROS and NO bioactivity involves post-translational modifications of proteins, particularly S-glutathionylation for ROS, and S-nitrosylation for NO. These changes may alter the activity, stability, and interaction with other molecules or subcellular location of proteins, changing the entire cell dynamics and contributing to the maintenance of homeostasis. However, despite the recent advances about the roles of ROS and NO in signaling cascades, many challenges remain, and future studies focusing on the signaling of these molecules in planta are still necessary.

Mineral nutrition and enzymatic adaptation induced by arsenate and arsenite exposure in lettuce plants.

Arsenate (As(V)) and arsenite (As(III)) contamination is able to interfere negatively on plant metabolism, promoting a reduction of nutrients uptake and transport and also an increase of reactive oxygen species (ROS) generation. However, some plants are considered tolerant against As exposure through the activation of defense mechanisms. Therefore, this study aimed to evaluate the effects of different As(V) and As(III) concentrations (0.0, 6.6, 13.2, 26.4 and 52.8 μmol L(-1)), on mineral nutrients concentration [calcium (Ca), magnesium (Mg), phosphorous (P), iron (Fe), manganese (Mg) and copper (Cu)], on membrane lipid peroxidation and also on the enzymes belonging to the antioxidant defense system [superoxide dismutase (SOD), total peroxidase (POX), catalase (CAT), glutathione reductase (GR) and ascorbate peroxidase (APX)] of plants of Lactuca sativa L. cv Hanson. As(V) and As(III), showed, in general, the same toxic effects in leaves and roots with significant changes in essential macro- and micronutrients concentration. Lipid peroxidation of cellular membranes was also observed in tested plants, probably resulted from an action of ROS generated by this metalloid. The increase of ROS generation and their scavenge were evident since an increase of SOD, POX, CAT and APX activity in leaves, and SOD, CAT and GR activity in roots were observed. Therefore, As(V) and As(III) exposure resulted in toxic effects in leaves and roots of lettuce plants; however, this plant species was able to attenuate these potential As damages through the activation of defense mechanisms, keeping its metabolism. Arsenic-tolerant plants are considered a great risk to the public health since it results in As insertion to the food chain.

Anthocyanins, thiols, and antioxidant scavenging enzymes are involved in Lemna gibba tolerance to arsenic

The influence of arsenic (As) on the growth and the antioxidant system of Lemna gibba L. exposed to five concentrations of As (0.0, 0.25, 0.5, 1.0, and 1.5 mg L−1) was studied. Although As exposure reduced relative growth rate, L. gibba continued to grow even after the high accumulation of this element after five days of exposure. The concentration of the superoxide anion was unaffected by As, whereas an increase of hydrogen peroxide concentrations was observed with the increasing of As concentration. Increasing concentrations of As also increased the enzyme activity of superoxide dismutase, peroxidase, and glutathione reductase and the total and nonprotein thiols, up to 0.5 mg L−1, whereas the anthocyanin content increased constantly with As concentration. Catalase and ascorbate peroxidase activities as well as the content of chloroplastic pigments were reduced in plants exposed to all As concentrations. These results support a major role of anthocyanins, nonprotein thiols, and antioxidant scavenging enzymes in L. gibba tolerance to toxic As concentrations.

Evaluation of the potential of Pistia stratiotes L. (water lettuce) for bioindication and phytoremediation of aquatic environments contaminated with arsenic

Specimens of Pistia stratiotes were subjected to five concentrations of arsenic (As) for seven days. Growth, As absorption, malondialdehyde (MDA) content, photosynthetic pigments, enzymatic activities, amino acids content and anatomical changes were assessed. Plant arsenic accumulation increased with increasing metalloid in the solution, while growth rate and photosynthetic pigment content decreased. The MDA content increased, indicating oxidative stress. Enzymatic activity and amino acids content increased at the lower doses of As, subsequently declining in the higher concentrations. Chlorosis and necrosis were observed in the leaves. Leaves showed starch accumulation and increased thickness of the mesophyll. In the root system, there was a loss and darkening of roots. Cell layers formed at the insertion points on the root stems may have been responsible for the loss of roots. These results indicate that water lettuce shows potential for bioindication and phytoremediation of As-contaminated aquatic environments.

Corrigendum: The Involvement of Nitric Oxide in Integration of Plant Physiological and Ultrastructural Adjustments in Response to Arsenic

High arsenic (As) concentrations are toxic to all the living organisms and the cellular response to this metalloid requires the involvement of cell signaling agents, such as nitric oxide (NO). The As toxicity and NO signaling were analyzed in Pistia stratiotes leaves. Plants were exposed to four treatments, for 24 h: control; SNP [sodium nitroprusside (NO donor); 0.1 mg L-1]; As (1.5 mg L-1) and As + SNP (1.5 and 0.1 mg L-1, respectively). The absorption of As increased the concentration of reactive oxygen species and triggered changes in the primary metabolism of the plants. While photosynthesis and photorespiration showed sharp decrease, the respiration process increased, probably due to chemical similarity between arsenate and phosphate, which compromised the energy status of the cell. These harmful effects were reflected in the cellular structure of P. stratiotes, leading to the disruption of the cells and a possible programmed cell death. The damages were attenuated by NO, which was able to integrate central plant physiological processes, with increases in non-photochemical quenching and respiration rates, while the photorespiration level decreased. The increase in respiratory rates was essential to achieve cellular homeostasis by the generation of carbon skeletons and metabolic energy to support processes involved in responses to stress, as well to maintaining the structure of organelles and prevent cell death. Overall, our results provide an integrated view of plant metabolism in response to As, focusing on the central role of NO as a signaling agent able to change the whole plant physiology.

Arsenic toxicity: cell signalling and the attenuating effect of nitric oxide in Eichhornia crassipes

Nitric oxide (NO) is an important molecule involved in the perception of stress induced by toxic compounds such as arsenic (As). The present study investigated the role of NO applied as sodium nitroprusside (SNP) in cell signalling and the ability of NO to attenuate the toxic effects of As (in the form of sodium arsenate) in water hyacinth (Eichhornia crassipes). Water hyacinth plants were collected and assigned to one of the following treatments: control; 100 μM SNP; 20 μM As; or 20 μM As + 100 μM SNP. The plants remained under these conditions for 0, 4, 12, and 24 h. After each time interval, the plants were collected and As absorption, production of reactive oxygen species (ROS), integrity of membranes, and antioxidant enzyme activities were evaluated. The plants were able to absorb and accumulate large amounts of As, even after only four hours of exposure to the pollutant. The absorption and bioaccumulation factor of As was even greater when plants were exposed to both As and SNP. The accumulation of As triggered increases in ROS production and cell membrane damage. In the presence of SNP, the tolerance index to As increased and damage was mitigated. Therefore, from the present work, it was possible to conclude that exogenous NO influenced the ability of plants to tolerate As; this finding has implications for phytoremediation in areas contaminated by As.

Uptake arsenic by plants: Effects on mineral nutrition, growth and antioxidant capacity

El Arsenico (As) es uno de los principales contaminantes ambientales y la fitorremediacion se presenta como una herramienta efectiva para retirar este elemento del medio ambiente. En el presente estudio se analizo la influencia de este elemento en el crecimiento, nutricion mineral y fotosintesis de Pistia stratiotes bajo siete concentraciones de As (0, 3, 7, 10, 13, 16 y 20 μM). Encontrandose gran afinidad de esta especie por el As, siendo que la absorcion de este elemento ocurre deforma rapida afectando la absorcion de nutrientes esenciales. En este sentido, la absorcion de Cu, Mn, Fe y P aumento hasta una concentracion de 13 μM de As, disminuyendo en el caso de las mayores concentraciones, entre tanto se observo una disminucion en la absorcion de Mg. No fueron observados efectos sobre la absorcion de K, Ca y Zn. A pesar que tanto la fotosintesis como el crecimiento fueron negativamente afectados por las diferentes concentraciones de As la planta consiguio mantener una tasa reducida de crecimiento hasta la concentracion de 13 μM. Esta situacion asi como las alteraciones observadas en la absorcion de nutrientes, probablemente este relacionada con el aumento en la capacidad antioxidativa de la planta, indicando una posible respuesta de resistencia de la planta frente a este elemento contaminante. De esta forma es probable concluir que P. stratiotes actua como una eficiente fitorre-mediadora de As, aun en concentraciones cien veces mayor que los niveles permitidos en el agua apta para consumo humano.