Hydrogen Peroxide, Signaling in Disguise during Metal Phytotoxicity

Abstract

Plants exposed to excess metals are challenged by an increased generation of reactive oxygen species (ROS) such as superoxide (O2•-), hydrogen peroxide (H2O2) and the hydroxyl radical (•OH). The mechanisms underlying this oxidative challenge are often dependent on metal-specific properties and might play a role in stress perception, signaling and acclimation. Although ROS were initially considered as toxic compounds causing damage to various cellular structures, their role as signaling molecules became a topic of intense research over the last decade. Hydrogen peroxide in particular is important in signaling because of its relatively low toxicity, long lifespan and its ability to cross cellular membranes. The delicate balance between its production and scavenging by a plethora of enzymatic and metabolic antioxidants is crucial in the onset of diverse signaling cascades that finally lead to plant acclimation to metal stress. In this review, our current knowledge on the dual role of ROS in metal-exposed plants is presented. Evidence for a relationship between H2O2 and plant metal tolerance is provided. Furthermore, emphasis is put on recent advances in understanding cellular damage and downstream signaling responses as a result of metal-induced H2O2 production. Finally, special attention is paid to the interaction between H2O2 and other signaling components such as transcription factors, mitogen-activated protein kinases, phytohormones and regulating systems (e.g. microRNAs). These responses potentially underlie metal-induced senescence in plants. Elucidating the signaling network activated during metal stress is a pivotal step to make progress in applied technologies like phytoremediation of polluted soils.

Rhizosphere pseudomonads as probiotics improving plant health

“…The volatility of such materials as butanediol, or effector movement through the plant, as demonstrated for AHSLs , could be involved in the systemic nature of the responses. Reactive oxygen species (ROS) output in plant cells contacted with the elicitors is speculated to be a primary signal (Cuypers et al, 2016;Hossain et al, 2015). For instance, phenazines stimulate ROS production in contacted cells through their electron shuttle potential (Briard et al, 2015).…”

Subcellular Compartmentalization and Chemical Forms of Lead Participate in Lead Tolerance of Robinia pseudoacacia L. with Funneliformis mosseae

“…Pb pollution may be naturally occurring or result from anthropogenic activities (Yadav, 2010), creating potential hazards to ecosystems (Lantzy and Mackenzie, 1979). Pb pollution has also been a serious threat to human health and food safety (Cuypers et al, 2016), especially harmful to young children (Datko-Williams et al, 2014). Over the last decade, evidence has been shown that Pb exposure-related health injury occur already at lower blood Pb levels than previously documented (Henry et al, 2015).…”

New insights about cadmium impacts on tomato: Plant acclimation, nutritional changes, fruit quality and yield

“…Decreases in Cd uptake can also be provided by soil microorganisms, which increases solubilization of nutrients that may compete with Cd in sites for its absorption and translocation (Dourado et al, 2013;Madhaiyan et al, 2007;Sebastian & Prasad, 2016a). In addition, some organisms from soil microbiological community can change plant response to Cd exposure by altering hormonal balance of plants, and by modifying generation of reactive oxygen species, which are important signaling molecules (Cuypers et al, 2016;Dourado et al, 2013;Madhaiyan et al, 2007).…”

“…Once within the plant, Cd triggers oxidative stress, disturbs nutrient uptake and distribution, impairs photosynthesis, triggers chromosomal aberrations, and decreases yield (Bayçu, Gevrek‐Kürüm, et al., ; Bayçu, Rognes, et al., ; Carvalho et al., ; Gallego et al., ; Gratão, Polle, Lea, & Azevedo, ; Gratão et al., ; Hédiji et al., ; Sebastian & Prasad, ,). Multiple studies have shown great damages in cell systems due to the overproduction of reactive oxygen and nitrogen species (the so‐called ROS and RNS, respectively) as a consequence of plant exposure to heavy metals (Alves et al., ; Branco‐Neves et al., ; Cuypers et al., ; Fidalgo, Freitas, Ferreira, Pessoa, & Teixeira, ; Fidalgo et al., ; Gallego et al., ; Iannone, Groppa, & Benavides, ). To a certain extent, plants can cope with the heavy metal‐induced oxidative stress by employing enzymatic and nonenzymatic antioxidant machineries, which encompass the modulation of superoxide dismutase (SOD, EC 1.15.1.1), catalase (CAT, EC 1.11.1.6), ascorbate peroxidase (APX, EC 1.11.1.11) activities, among other enzymes, as well as the synthesis of amino acids, soluble sugars, glutathione, and their derivates (Cuypers et al., ; Gallego et al., ; Jozefczak, Remans, Vangronsveld, & Cuypers, ; Méndez, Pena, Benavides, & Gallego, ; Štolfa, Pfeiffer, Špoljarić, Teklić, & Lončarić, ).…”

“…Physicochemical characteristics of the soil, such as pH, texture, and organic matter content, affect Cd availability for plant absorption, which is particularly enhanced under acidic conditions (Castaldi & Melis, 2004;Kabata-Pendias, 2011;Kibria, Osman, & Ahmed, 2006;Manciulea & Ramsey, 2006;Melo, Alleoni, Carvalho, & Azevedo, 2011;Nogueirol, Monteiro, Gratão, Silva, & Azevedo, 2016). Furthermore, soil microorganisms may influence Cd uptake as well as its effects on tomato plants (1) by changing availability of nutrients that, in addition to be necessary to the plant development, may compete with Cd in sites for absorption and/or translocation, (2) by modifying hormonal balance in plants, and (3) by modulating the production of reactive oxygen species, which are important signaling molecules (Cuypers et al, 2016;Dourado et al, 2013;Madhaiyan, Poonguzhali, & Sa, 2007;Sebastian & Prasad, 2016a). In addition, similar to nutrients (Alvarenga, 2013), the uptake of nonessential elements may be enhanced in plants that were grown in hydroponic systems in comparison to soil.…”