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Plant Signaling & Behavior logoLink to Plant Signaling & Behavior
. 2013 Jan 18;8(3):e23425. doi: 10.4161/psb.23425

Transition metals

A double edge sward in ROS generation and signaling

Ana Rodrigo-Moreno 1, Charlotte Poschenrieder 2, Sergey Shabala 3,*
PMCID: PMC3676510  PMID: 23333964

Abstract

Transition metals such as Iron (Fe) and Copper (Cu) are essential for plant cell development. At the same time, due their capability to generate hydroxyl radicals they can be potentially toxic to plant metabolism. Recent works on hydroxyl-radical activation of ion transporters suggest that hydroxyl radicals generated by transition metals could play an important role in plant growth and adaptation to imbalanced environments. In this mini-review, the relation between transition metals uptake and utilization and oxidative stress-activated ion transport in plant cells is analyzed, and a new model depicting both apoplastic and cytosolic mode of ROS signaling to plasma membrane transporters is suggested.

Keywords: copper, iron, membrane transport, potassium, calcium, hydroxyl radicals, oxidative stress, toxicity, adaptation, development


Recently, reactive oxygen species (ROS) have emerged as important signaling molecules mediating a broad range of plant adaptive and developmental responses. In plant cells, both photosynthetic and respiratory electron-transport chains, as well as the NADPH oxidases and peroxidases are involved in ROS generation.1 ROS have been shown to regulate gene expression and signaling transduction pathways and, as such, can control numerous processes, like root gravitropism, hypersensitive response to pathogens, stomatal closure and cell expansion and development.1-5 During pathogen attack, programmed cell death (PCD) is induced in order to isolate cells and therefore avoiding pathogen spread. ROS play a crucial role in this signaling network.6 In many cases, ROS production is genetically programmed and is induced during development. Generation of singlet oxygen induces controlled PCD in aleurone cells, leaf senescence, tracheary elements maturation or trichome development.4

While ROS control over numerous adaptive and developmental responses is absolutely essential, a controlled balance of ROS-producing and ROS-scavenging systems must be kept to ensure an accurate execution of signaling without provoking toxicity. Several types of ROS may be formed in plant cells. These forms can be poorly reactive (non-radicals, such as H2O2 or O3) or can react extremely quickly with other free radicals such as superoxide (O2-) or hydroxyl radicals (OH·)7; see also Figure 1. The detrimental effects of ROS are a result of their ability to cause lipid peroxidation in cellular membranes, DNA damage, protein denaturation, carbohydrate oxidation, pigment breakdown and an impairment of enzymatic activity.8,9 To protect cells against oxidative injury plants use various antioxidant components a number of enzymes and low molecular weight compounds capable of quenching ROS without themselves undergoing conversion to a destructive radical.8 Antioxidant defense includes enzymatic and non-enzymatic mechanisms. The first group includes the enzymes superoxide dismutase (SOD), ascorbate peroxidase (APX) and glutathione peroxidase. The second group includes cellular redox buffers such as ascorbate, glutathione (GSH), tocopherol, flavonoids, alkaloids and carotenoids.1

graphic file with name psb-8-e23425-g1.jpg

Figure 1. ROS production by multistep reduction of oxygen (adapted from refs.1 and 4). Grey lines show the Haber-Weiss reactions. TM, transition metal.

Transition metals such as iron (Fe), manganese (Mn), zinc (Zn) or copper (Cu) are classified as essential micronutrients and act as cofactors of many fundamental proteins in plant cells. Among many roles, each of them may be included as a metal component of the prosthetic group in superoxide dismutases (SOD) and, thus, plays central role in detoxification of the superoxide anion free radicals.10,11 SODs are present in all subcellular compartments: FeSODs are localized in chloroplasts, MnSODs are present in both mitochondrion and peroxisomes and Cu/ZnSODs, the type of SOD predominant in plant cells, are localized in chloroplasts, peroxisomes, cysosol and extracellular space (reviewed in ref.12). As a result, deficiency in one of these micronutrients can alter the activities of antioxidant enzymes resulting in increased susceptibility to oxidative stress.13

The standard electrode potential is an excellent predictor of both the prooxidant activity and the toxicity of metal ions.14 While Zn and Mn have no or very little reducing potential under biological conditions,15 Fe and Cu are highly redox active (and, hence, potentially toxic) metals. If they are not chelated, at every concentration they can mediate ROS production by getting oxidized in the Fenton reaction and further getting reduced in the net Haber-Weiss reactions (Fig. 1). The production of ROS by Cu and Fe ions by the Fenton reaction can occur in plant cells in presence of ascorbate or H2O2,16 leading to the production of hydroxyl radicals.7 To deal with Fe- or Cu- induced toxicity, plants need to enhance antioxidant defenses; this phenomenon has been reported for a wide range of species such as Nicotiana plumbagnifolia,17 Phaseolus vulgaris,18Ulva compressa,19 Zea mays20 or Arabidopsis thaliana.21

This essentiality/toxic duality of transition metals has resulted in the development of a complex homeostatic network for their acquisition and use in aerobic organisms.22-25 In Arabidopsis thaliana, primary root uptake of the transition metals includes members of different families: NRAMP, ZIP and COPT (Table 1). In all cases, the transport is induced under limiting conditions of the transition metals and in all cases, these transporters can mediate the influx of more than one transition metal. Interestingly, β-glucuronidase (GUS) expression pattern of these transporters reveals a possible specialization of the different root zones in the acquisition of the different essential micronutrients: AtCOPT1, responsible of high affinity copper transport, is located at root tip;26 AtNRAMP1, that mediates Mn transport, is highly expressed at the elongation zone.27 In relation to ZIP family transporters (IRT1-3 and ZIP1-4), responsible of both Fe and Zn transport, AtIRT1, responsible of Fe transport, and AtZIP4, that mediates Zn transport, are mainly located at the mature zone level.28,29

Table 1. Transporters implicated in primary uptake of TM in Arabidopsis.

High affinity transporter Expression under limiting conditions? Expression pattern in roots Main ion transported Also transports References
AtNRAMP1
+
Plasma membrane.Higher expression at the elongation zone level
Mn
Fe, Co
27,49
AtIRT1
+
Plasma membrane. External cell layers of the mature zone.
Fe
Zn, Mn, Cd, Co
28,5051
AtIRT2
+
Epidermis, root hairs and cortex. Absent in root apex
Fe*
Zn*
52
AtIRT3
+
Plasma membrane. Vascular tissues. Absent at the elongation zone
Zn*
Fe*
53
AtZIP1-3
+
 
Zn
Cu (ZIP2)
54
AtZIP4
+
Whole roots?
Zn*
Cu*
29,54
COPT1 + Plasma membrane. Root apex Cu Ag, Mn 26,5556
*

Based on expression in yeast data.

While membrane transporters are essential for acquisition of transition metals, they may also represent a downstream target of ROS signaling. The activation of plasma membrane calcium influx by ROS in plant cells has been a hot topic during the last decade resulting in multiple publications.30-37 This activation shows high spatial- and dose-dependence, and varies with the type of ROS.33-37

Of specific interest is ROS-induced K+ efflux. The latter has been reported in most of the abiotic stresses that imply ROS generation, such as copper37,38 or Al toxicity,39,40 salinity,33,42 and waterlogging.43,44 The first evidence of ROS-induced activation of K+ -permeable conductance was reported in combined patch-clamped and MIFE experiments by Demidchik et al.35 The underlying molecular mechanisms were studied later in more details, by comparing ROS-induced activation of K+ currents and fluxes between Arabidopsis wild type and gork1-1 mutants. This study revealed that, similarly to animal cells, hydroxyl radicals-activated K+ channels are involved in programmed cell death in plant cells.33 Recently, Lahoavist et al.36 showed that the hydroxyl-radical activated Ca2+ and K+ conductance in Arabidopsis is mediated by annexin1 at the mature and elongation zone levels. In all these studies, the hydroxyl radical generation occurred at the external side of the plasma membrane, and under non-physiological (1mM of the hydroxyl-radical generation mixture Cu/Asc) conditions.

Using a range of Arabidopsis loss- or gain- of Cu transport function mutants,37 we have recently showed that copper transport into cytosol in root apex results in generation of hydroxyl radical at the cytosolic side, with a consequent regulation of plasma membrane OH-sensitive Ca2+ and K+ transport systems. Based on stoichiometry between Ca2+ and K+ fluxes and pharmacological experiments evidence, non-selective cation channels (NSCC) have been suggested as a possible target. Such cytosolic activation of NSCC by hydroxyl radicals has been previously shown for animal cells45 but not in plant cells. Keeping in mind high tissue-specificity of expression patterns of transporters mediating uptake of transition metals into plant roots (see Table 1), this finding may explain specificity or ROS effects in different root tissues, both in adaptive5,46,47 and developmental4,48 context.

While much more work is needed to completely understand the catalytic role of these transient metals in ROS-mediated responses in plants, and their impact on intracellular ionic homeostasis, there is no doubt that our current models depicting ROS generation under stress conditions in plant roots must be updated to include both apoplastic and cytosolic modes of action (Fig. 2). This model also highlights a complex role transition metals play in ROS generation and signaling in plants. On one hand, they are essential components of plant antioxidant defense system and, as such, are involved in ROS scavenging (e.g., as a part of SOD). On the other hand, both Cu and Fe may be directly involved in ROS production, both in the apoplast and the cytosol (Fig. 2). This “double sward” action should be finely balanced to optimize plant adaptive and developmental performance. The fine print of this balancing process must be a subject of dedicated research in the future. (Ref. 41; Fig. 3)

graphic file with name psb-8-e23425-g2.jpg

Figure 2. Suggested model for hydroxyl radical generation by transition metals and activation of ion transport systems under low copper or iron conditions. Low transition metal (TM) concentrations in the cytosol induce activity of the plasma membrane high affinity COPT1 and IRT1 transporters.1 These transporters mediate Cu and Fe transport into the cytosol.2 Cytosolic TM are then transported to metallochaperones for essential functions in major plant organelles.3 as well as to cytosolic-located SOD enzymes.4 A small part of the TM generates moderate OH in the cytosol5 that will activate Ca2+ entry through NSCC6 at the root tip level.37 This cytosolic calcium increase is essential for root tip growth.7,48 Abbreviations: COPT1, high affinity copper transporter 1; IRT-3, iron-regulated transporter 1; NSCC, non-selective cation channel; SOD, superoxide dismutase.

graphic file with name psb-8-e23425-g3.jpg

Figure 3. Hydroxyl radical generation and activation of ion transport systems under high copper or iron conditions. When TM are present in excessive quantities in soil solution, they are transported into cytosol through ZIP transporters1 where they will interact with cytosolic H2O2 to generate OH.2 The latter will activate NSCC-mediated Ca2+ uptake3 in root tips.37 The resultant increase in cytosolic Ca2+ pool will further increase net Ca2+ uptake into cytosol via positive feedback regulation of NADP(H)oxidase57 and production of extracellular H2O2.4 The latter may interact with TM in the cell walls in the presence of ascorbic acid, to produce substantial quantities of OH in apoplast.5 This apoplastic OH could activate ANN1-mediated Ca2+ and K+ conductances6 at both mature and elongation zones36 resulting in further increase in cytosolic Ca2+ (hence, a positive feedback loop) and decline in cytosolic K+ pool. Apoplastic peroxide produced as a result of NADP(H) oxidase stimulation will be also transported in the cytosol via aquaporins, further increasing cytosolic OH levels by interacting with TM.2 Apoplastic OH generation will also stimulate K+ leak via outward-rectifying K+ GORK channel,7,33 further reducing cytosolic K+ pool. OH generated in the cytosol will also contribute to this process by activating NSCC from cytosolic site.8,37 The massive decrease in cytosolic K+ pool (mediated by Ann1, GORK and NSCC channels) will result in activation of various proteases and nucleases,9,33,42,58 leading to programmed cell death.10 Abbreviations: ZIP, Zrt-, Irt-like protein; NSCC, non-selective cation channel; ANN1, Annexin 1; NADP(H), oxidase (Nicotinamide Adenine Dinucleotide Phosphate-Oxidase); PCD, programmed cell death; AQ, aquaporin.

Acknowledgments

This work has been supported by the Spanish MICINN (Projects BFU2007-60332 and BFU2010-14873). A.R-M. acknowledges her PhD fellowship from Ministerio de Ciencia e Innovación (BES-2008-005096). S.S. acknowledges financial support from the Australian Research Council. The authors would like to thank Lola Peñarrubia for their critical revision of the manuscript.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Footnotes

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