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Regulatory networks of cadmium stress in plants

Regulatory networks of cadmium stress in plants REVIEW REVIEW Plant Signaling & Behavior 5:6, 663-667; June 2010; © 2010 Landes Bioscience Giovanni DalCorso, Silvia Farinati and Antonella Furini* Università degli Studi di Verona; Dipartimento di Biotecnologie; Verona, Italy Key words: cadmium detoxification, heavy metal stress, phytoremediation, signal transduction, transcription factors for lowering the photosynthetic quantum yield. In addition, Cd During their life, plants have to cope with a variety of abiotic decreases carbon assimilation by inhibiting enzymes involved in stresses. Cadmium is highly toxic to plants, water soluble CO fixation. In several plant species, Cd toxicity is manifested and therefore promptly adsorbed in tissues and its presence at cellular level as chromosomal aberrations and alteration of cell greatly influences the entire plant metabolism. In this review, cycle and division. High mutation rate and malformed embryos we focus on the signal pathways responsible for the sensing have been observed in Arabidopsis plants exposed to Cd. and transduction of the “metal signal” inside the cell, ultimately Plant molecular response to Cd stress is characterized by driving the activation of transcription factors and consequent expression of genes that enable plants to counteract the heavy the synthesis of stress-related proteins and signaling molecules. metal stress. Phytosiderophores, nicotianamine and organic acids are a few examples of chelating compounds that are released by roots and might inu fl ence heavy metals uptake. Functional genomics tech - nologies have recently increased our knowledge of the complex In order to respond to stress signals, plant cells must be able to per- regulatory networks associated with Cd stress in plants. In this ceive these signals and convert them into appropriate responses, article we review recent progress on the molecular component of which in turn confer on plants the ability to tolerate unfavorable the Cd-induced signal transduction that triggers the activation of conditions. Plant tolerance mechanisms require a coordination genes responsible for Cd uptake, transport and detoxification. of complex physiological and biochemical processes, including changes in global gene expression, protein modification and pri - Cadmium Stress: From Sensing to Gene Activation mary and secondary metabolite compositions. In the last decade functional genomics approaches have partially unraveled the Signal transduction pathways. In whole plants, roots are the complex mechanisms that drive from stress perception and trans- primary site through which heavy metals gain access. Analysis duction, through a cascade of signaling molecules, to the expres- of the Cd and Cu localization under an electron microscope, sion modulation of genes responsible for plant stress response. for instance, showed that the root cell wall, in comparison with In addition, the elucidation of the function of newly identified the cytoplasm, contains the majority of heavy metals. Indeed, stress-responsive non-coding RNA will facilitate understanding because of their negative charge, cell walls have a significant 3 14 of the complex response to stress. capacity for heavy metal binding and retention. Cell walls have Soil and water pollution by heavy metals is a serious environ- acquired importance as active metabolic sites, where a variety of mental problem. Although heavy metals occur naturally in soil signaling molecules are generated in response to extra-cellular as rare elements, agricultural practices, refuse dumping, metal- stimuli. The finding that proteins directed to the apoplastic space lurgy and manufacturing all contribute to their spread in the are synthesized in response to Cd and Ni exposure is noteworthy, environment. Among heavy metal pollutants, cadmium (Cd) is pointing out an important role of the cell wall as a prime heavy considered to be one of the most phytotoxic. Because of its high metal-sensing site. solubility in water, it is promptly taken up by plants and this rep- Gene expression patterns change in response to toxic elements. resents the main entry pathway into the food chain, also causing After sensing the heavy metal, the plant cell activates specific serious problems to human health. Even at low concentrations, genes to counteract the stress stimuli. A signal transduction cas- the uptake by roots and transport to the vegetative and reproduc- cade is therefore responsible for the differential gene regulation. In tive organs has a negative effect on mineral nutrition and homeo- eukaryotes, mitogen-activated protein kinase (MAPK) pathways 5-7 stasis in plant shoot and root growth and development. represent a signaling mechanism that consists of three sequentially Evident symptoms of Cd toxicity are leaf rolling and chlorosis, activated protein kinases: MAPK kinase kinase (MAPKKK), 8 16,17 water uptake imbalance and stomatal closure. Cd damages the MAPK kinase (MAPKK), and MAPK. MAPKKKs are photosynthetic apparatus and causes a decrease in chlorophyll and Ser/Thr protein kinases that phosphorylate MAPKKs. Once carotenoid content. Together, these Cd effects are responsible phosphorylated, and therefore activated, MAPKKs are respon- sible for the phosphorylation of MAPKs on Thr and Tyr residues. This phosphorylation renders these enzymes active. MAPKs *Correspondence to: Antonella Furini; Email: [email protected] Submitted: 02/05/10; Accepted: 02/05/10 are able to phosphorylate numerous substrates in different cel- Previously published online: lular compartments, among which, transcription factors. In www.landesbioscience.com/journals/psb/article/11425 plants, the MAPK cascade is involved in response to a variety www.landesbioscience.com Plant Signaling & Behavior 663 Figure 1. Representation of the transduction pathway involved in Cd signaling. (A) Once entered the plant cell Cd induces ROS, responsible for the activation of MAPK kinase cascade. This, together with the activation of Ca-calmodulin system and stress-related hormones, converge regulating transcription factors in the nucleus. (B) In turn, transcription factors induce expression of Cd-detoxification responsible genes. JA (jasmonic acid); SA (salicylic acid); ROS (reactive oxygen species); MAK (mitogen-activated protein kinase); TF (transcription factor); PC (phytochelatin); PCS (phytochelatin synthetase); MT (metallothionein). 18 20 of environmental, hormonal and developmental stimuli. It has heavy metal signaling has also been hypothesized. Indeed, Ca recently been shown that stress due to excessive Cd (and Cu) acti- concentration in cells greatly increases during Cd stress and it vates different kinase enzymes belonging to the MAPK family. stimulates calmodulin-like proteins that interact with Ca ions. The phosphorylation cascade is therefore thought to be involved Changing their conformation in response to Ca binding, calm- in Cd signaling to the nucleus (Fig. 1A). odulin proteins regulate a variety of mechanisms, including ion Calcium ions and calmodulin are well-known second messen- transport, gene regulation, metabolism and stress tolerance that gers of external stimuli, and the participation of this system in coordinate, at least in part, the plant response to Cd. The Ca/ 664 Plant Signaling & Behavior Volume 5 Issue 6 calmodulin system is also involved in sensing other heavy metals, Cd ions is rather slower than to Cu. This could be due to the fact and in fact, transgenic plants expressing a tobacco calmodulin-like that Cd stimulates an oxidative stress as a secondary effect, which protein exhibit increased Ni tolerance and Pb accumulation. is responsible for the MAPKs activation, delaying the phospho- Another mechanism that is thought to be involved in Cd sens- rylation cascade. ing is the reduced glutathione-oxidized glutathione ratio (GSH/ Summarizing, heavy metal stress signals appear to be trans- GSSG). Glutathione can control the differential expression of duced through a variety of pathways that overlap and cross-talk. antioxidant enzymes, such as chalcone synthase, phenylalanine Activation of phosphorylation cascades, Ca-calmodulin system, ammonia lyase, superoxide dismutase or glutathione reductase, ROS signaling and stress-related hormones eventually converge usually induced by heav y metal stress. During Cd stress, a reduc- regulating transcription factors that are deputed to the activation tion in GSH/GSSG ratio has been observed in different plant of gene sets responsible for response to stress (Fig. 1A). species, with the consequent activation of the response genes. Modulation of transcription factors. Transcriptomic changes Regulation in hormone synthesis has also been observed dur- upon Cd stress have been investigated in several plant species, 29,30 24 31 ing heavy metal stress. Treatments with Cd or Cu, for instance, including Arabidopsis, pea and barley. This analysis led enhance jasmonic acid content in Arabidopsis, Oryza and bean. to the identification of numerous transcription factors (TFs), 32-34 Ethylene synthesis is also increased upon treatment with Cd, Cu, involved in Cd plant response. Fe, Zn, and in the case of Cd and Cu, this increase is due to an Cd-responsive TFs share the same signal transduction path- upregulation of ACC synthase transcription and enhanced activ- way with other stress-related TFs, and can therefore be acti- ity. Salicylic acid (SA) is another well-known hormone involved vated by other abiotic stresses such as cold, dehydration, SA and in stress signaling in plants and exposure to Cd has been shown H O . Moreover, the modulation of TFs belonging to several 2 2 to stimulate SA accumulation in roots. All these data together families demonstrates the complexity of the response of plants to 32 36 suggest that cross-talk exists between heavy metal signaling and Cd stress. TFs belonging to different families, such as WRK Y, 37 38 biotic stress signaling. It has been shown that a mild exposure basic leucine Zipper (bZIP), ethylene-responsive factor (ERF) to heavy metals can induce greater plant resistance against viral and myeloblastosis protein (MYB) play a significant role in and fungal infections without being connected to the direct toxic controlling the expression of specific stress-related genes after Cd effect of the metal. Conversely, application of SA on barley seed- treatment. lings before Cd treatment caused partial protection against the Cd regulates the expression of ERF proteins (e.g., ERF1 and 25 30 heavy metal toxicity. ERF2, ) belonging to the APETALA2 (AP2)/ethylene-respon- Hormone signaling is not the only example of redundancy sive-element-binding protein (EREBP) family and is also able to between heavy metal and (a)biotic stress. The signal mediated by bind to several pathogenesis-related promoters and dehydration Reactive Oxygen Species (ROS) is also reported. In fact, heavy responsive elements (DRE). An example of TF induced by Cd metal stress triggers the accumulation of ROS both directly, via and binding to DR E motif is DR EB2A: it can specifically interact Fenton or Haber-Weiss reaction and indirectly, unbalancing the with the promoter region of the Rd29A (desiccation responsive) activity of antioxidative enzymes, as in the case of Cd. H O gene, on the DRE motif, inducing the transcription of Rd29A 2 2 plays a role as signal molecule inducing defense mechanisms after Cd-exposure. against both abiotic stresses, such as temperature and ozone, In addition, it was observed that MYB4 is highly expressed 27 34 and pathogen attack. Based on the evidence that both heavy after Cd and Zn treatment in A. thaliana, while MYB43, metal stress and ROS-mediated biotic stress induce phytoalex- MYB48 and MYB124 proteins are specifically induced by Cd in ins biosynthesis, it has been hypothesized that heavy metal and roots. Furthermore, the TFs MYB72 and bHLH100 (belong- biotic stress response share common signals. It remains anyway ing to the helix-loop-helix TFs group) were studied for their doubtful whether the effects of heavy metals on plants should be implication in metal homeostasis because they showed an altered attributed to their direct effect on membranes, cellular enzymes expression after Cd exposure. In Cd-treated Thlaspi caerulescens 34,36 and photosynthetic apparatus or to their indirect effect caused by MYB28 and WRKY53 are strongly expressed, even if the lat- the induction of some signaling pathways that are responsible for ter has been supposed to be involved in the signal transduction the so called heavy-metal stress response. pathway regulating the activity of other TFs. It is noteworthy that plant cells probably transduce heavy OBF5, belonging to the bZIP group, regulates the expression metal signaling in different ways for different heavy metals. The of glutathione S-transferase binding to its promoter region in a main differentiation is probably due to the fact that some metals Cd-induced manner. TGA3 protein also has a putative role in do not have any known function and could induce deleterious modulating gene expression upon Cd-treatment, as well as in effects even at low concentration. Conversely, other metal ions response to biotic stress. Recently, BjCdR15, orthologous to take part in the normal cell metabolism and are shown to be toxic TGA3, has been identified in B. juncea after short Cd treatment; only at high concentrations. A good example of this is the activa- BjCdR15 inu fl ences the expression of several metal transporters, tion of the phosphorylation cascade of MAPK proteins induced being therefore involved in long distance root-to-shoot Cd trans- 7,32 by Cu and Cd. Cu stress rapidly activates SIMK, MMK2, port. In addition, its overexpression in A. thaliana and tobacco MMK3 and SAMK kinases, and their activation is probably enhances Cd tolerance and accumulation in shoots. 19 40 the consequence of oxidative stress generated by the metal ion. Finally, other TFs named metal-responsive TFs (MTFs), Conversely, activation of the above-cited MAPKs in response to control the expression of metallothioneins by binding metal- www.landesbioscience.com Plant Signaling & Behavior 665 41 regulatory elements (MREs) in their promoter region. MTF-1, and Cd ions are bound to the thiolic groups of Cys. Cd-PCs com- for instance, was first identified as a Zn dependent MR E-binding plexes are transported into the vacuoles where they pack to form 42 8,51 factor essential for Zn and Cd dependent induction of the high-molecular-weight complexes (Fig. 1B). PCs also play a murine MT-I and MT-II genes. role in long-distance Cd transport from root to shoot: this would Activation of metal transporters. Once Cd has entered the contribute towards keeping Cd accumulation low in the root, cells, plants use various strategies to cope with its toxicity. One causing extra Cd transport to the shoot. such strategy consists of transporting Cd out of the cell or seques- Genes encoding PCS have been cloned from different organ- tering it into the vacuole, thereby removing it from the cytosol. isms, for example, OsPCS1, TaPCS1, AtPCS1 and CePCS1 Members of different transporter families contribute to Cd resis- from rice, wheat, Arabidopsis and Caenorhabditis elegans respec- 8,56,57 tance. The ABC transporter AtPDR8 has been shown to medi- tively, and BjPCS1 from the metal-tolerant plant Brassica ate Cd extrusion out of the plasma membrane of root epidermal juncea. Experimental data confirmed that accumulation and cells. Detoxification of Cd is also achieved by members of the tolerance to Cd is increased in transgenic plants overexpress- ZIP (ZRT, IRT-like protein) family. They are plasma-membrane ing PCS. In B. juncea, enhanced tolerance to Cd, As and Zn proteins induced in roots and shoots of Arabidopsis in response to was associated to the overexpression of AtPCS. However, an Zn-limiting conditions, and being involved in the xylem upload- excessive expression of AtPCS caused hypersensitivity to Cd in ing process, are potentially implicated in Cd root-to-shoot trans- Arabidopsis plants. port. IRT1 is essential for root iron uptake in response to iron Fina lly, meta llothioneins (MTs) are low-molecular-weight Cys- deficiency but it also accepts Cd as a substrate. HMA4, a mem- rich peptides also able to bind metal ions, such as Cd. Differently ber of the P-type metal ATPase, functions as Zn/Cd transporter from PCs, MTs are products of mRNA translation, induced in and by loading Cd into the xylem, it increases translocation to response to heavy metal stress. Binding to Cd, MTs also con- 47,48 the shoot where Cd might have less damaging effects. Another tribute to detoxifying the cytosolic environment from Cd toxic- family of metal transporters implicated in the mobilization of ity (Fig. 1B). Indeed, it has been reported that overexpression of Cd is the NRAMP (natural resistance-associated macrophage mouse MT in tobacco plants enhances Cd tolerance in vitro, protein). Indeed, expression of AtNRAMP1, AtNRAMP3 and whereas the Arabidopsis MT2a and MT3 increased Cd tolerance AtNR AMP4 in yeast showed that these proteins are able to trans- when expressed in Vicia faba. Moreover, B. juncea MT2 confers 49 64 port Cd. Recently, it was suggested that AtNR AMP6 functions increased tolerance to Cd and Cu in transgenic A. thaliana. In inside the cell either by mobilizing Cd from its storage compart- a recent study on hybrid Populus, it was shown that high levels of ment or by taking up Cd into a cellular compartment where it is MT2b correlated with Cd and Zn concentrations, demonstrating toxic. Finally, transporters of the CDF (cation diffusion facilita- that increased MT2b expression is one of the plant responses to tor) family appear to mediate the cytoplasmic efu fl x and vacuolar chronic metal exposure. sequestration of divalent metal cations such as Zn, Cd, Co, Ni or Mn. Conclusions and Perspectives Biosynthesis of chelating compounds. In the cell, Cd is che- lated by thiol-containing ligands such as glutathione (GSH) Heavy metal pollution is a significant environmental problem and its derivative phytochelatins (PCs), to allow the transport that is nowadays being evaluated as a major threat to humans. of Cd-complexes into the vacuole or in the apoplast by ATP- Researchers are concerned in developing new technologies for low dependent membrane pumps. GSH is required for PCs syn- cost and environmentally friendly land reclamation techniques. thesis. This process is catalyzed by the cytosolic PCs synthetase Increasing our knowledge about the mechanisms that enable (PCS). It has been shown that PCS is constitutively expressed, plants to cope with heavy metal stress would help in creating new but post-translationally activated by heavy metals. A recent tools applicable in phytoremediation, which is any technology study confirms that PCS is regulated by a Cd-dependent phos - that uses plants to reclaim polluted soils and waters. It is therefore phorylation on a Thr residue next to the catalytic site, and it of primary importance to further dissect the processes of heavy could therefore function as a “Cd sensor”. PCs have the gen- metal detoxification and signaling pathways in plants, to identify eral structure (γ-Glu-Cys)n-X (where n is a variable number from useful targets for biotechnological applications to increase plant 2 to 11 and X an amino acid such as Gly, β-Ala, Ser, Glu or Gln) t fi ness in heavy metal polluted sites. 4. Buchet JP, Lauwerys R, Roels H, Bernard A, Bruaux P, 8. Clemens S. 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Regulatory networks of cadmium stress in plants

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Abstract

REVIEW REVIEW Plant Signaling & Behavior 5:6, 663-667; June 2010; © 2010 Landes Bioscience Giovanni DalCorso, Silvia Farinati and Antonella Furini* Università degli Studi di Verona; Dipartimento di Biotecnologie; Verona, Italy Key words: cadmium detoxification, heavy metal stress, phytoremediation, signal transduction, transcription factors for lowering the photosynthetic quantum yield. In addition, Cd During their life, plants have to cope with a variety of abiotic decreases carbon assimilation by inhibiting enzymes involved in stresses. Cadmium is highly toxic to plants, water soluble CO fixation. In several plant species, Cd toxicity is manifested and therefore promptly adsorbed in tissues and its presence at cellular level as chromosomal aberrations and alteration of cell greatly influences the entire plant metabolism. In this review, cycle and division. High mutation rate and malformed embryos we focus on the signal pathways responsible for the sensing have been observed in Arabidopsis plants exposed to Cd. and transduction of the “metal signal” inside the cell, ultimately Plant molecular response to Cd stress is characterized by driving the activation of transcription factors and consequent expression of genes that enable plants to counteract the heavy the synthesis of stress-related proteins and signaling molecules. metal stress. Phytosiderophores, nicotianamine and organic acids are a few examples of chelating compounds that are released by roots and might inu fl ence heavy metals uptake. Functional genomics tech - nologies have recently increased our knowledge of the complex In order to respond to stress signals, plant cells must be able to per- regulatory networks associated with Cd stress in plants. In this ceive these signals and convert them into appropriate responses, article we review recent progress on the molecular component of which in turn confer on plants the ability to tolerate unfavorable the Cd-induced signal transduction that triggers the activation of conditions. Plant tolerance mechanisms require a coordination genes responsible for Cd uptake, transport and detoxification. of complex physiological and biochemical processes, including changes in global gene expression, protein modification and pri - Cadmium Stress: From Sensing to Gene Activation mary and secondary metabolite compositions. In the last decade functional genomics approaches have partially unraveled the Signal transduction pathways. In whole plants, roots are the complex mechanisms that drive from stress perception and trans- primary site through which heavy metals gain access. Analysis duction, through a cascade of signaling molecules, to the expres- of the Cd and Cu localization under an electron microscope, sion modulation of genes responsible for plant stress response. for instance, showed that the root cell wall, in comparison with In addition, the elucidation of the function of newly identified the cytoplasm, contains the majority of heavy metals. Indeed, stress-responsive non-coding RNA will facilitate understanding because of their negative charge, cell walls have a significant 3 14 of the complex response to stress. capacity for heavy metal binding and retention. Cell walls have Soil and water pollution by heavy metals is a serious environ- acquired importance as active metabolic sites, where a variety of mental problem. Although heavy metals occur naturally in soil signaling molecules are generated in response to extra-cellular as rare elements, agricultural practices, refuse dumping, metal- stimuli. The finding that proteins directed to the apoplastic space lurgy and manufacturing all contribute to their spread in the are synthesized in response to Cd and Ni exposure is noteworthy, environment. Among heavy metal pollutants, cadmium (Cd) is pointing out an important role of the cell wall as a prime heavy considered to be one of the most phytotoxic. Because of its high metal-sensing site. solubility in water, it is promptly taken up by plants and this rep- Gene expression patterns change in response to toxic elements. resents the main entry pathway into the food chain, also causing After sensing the heavy metal, the plant cell activates specific serious problems to human health. Even at low concentrations, genes to counteract the stress stimuli. A signal transduction cas- the uptake by roots and transport to the vegetative and reproduc- cade is therefore responsible for the differential gene regulation. In tive organs has a negative effect on mineral nutrition and homeo- eukaryotes, mitogen-activated protein kinase (MAPK) pathways 5-7 stasis in plant shoot and root growth and development. represent a signaling mechanism that consists of three sequentially Evident symptoms of Cd toxicity are leaf rolling and chlorosis, activated protein kinases: MAPK kinase kinase (MAPKKK), 8 16,17 water uptake imbalance and stomatal closure. Cd damages the MAPK kinase (MAPKK), and MAPK. MAPKKKs are photosynthetic apparatus and causes a decrease in chlorophyll and Ser/Thr protein kinases that phosphorylate MAPKKs. Once carotenoid content. Together, these Cd effects are responsible phosphorylated, and therefore activated, MAPKKs are respon- sible for the phosphorylation of MAPKs on Thr and Tyr residues. This phosphorylation renders these enzymes active. MAPKs *Correspondence to: Antonella Furini; Email: [email protected] Submitted: 02/05/10; Accepted: 02/05/10 are able to phosphorylate numerous substrates in different cel- Previously published online: lular compartments, among which, transcription factors. In www.landesbioscience.com/journals/psb/article/11425 plants, the MAPK cascade is involved in response to a variety www.landesbioscience.com Plant Signaling & Behavior 663 Figure 1. Representation of the transduction pathway involved in Cd signaling. (A) Once entered the plant cell Cd induces ROS, responsible for the activation of MAPK kinase cascade. This, together with the activation of Ca-calmodulin system and stress-related hormones, converge regulating transcription factors in the nucleus. (B) In turn, transcription factors induce expression of Cd-detoxification responsible genes. JA (jasmonic acid); SA (salicylic acid); ROS (reactive oxygen species); MAK (mitogen-activated protein kinase); TF (transcription factor); PC (phytochelatin); PCS (phytochelatin synthetase); MT (metallothionein). 18 20 of environmental, hormonal and developmental stimuli. It has heavy metal signaling has also been hypothesized. Indeed, Ca recently been shown that stress due to excessive Cd (and Cu) acti- concentration in cells greatly increases during Cd stress and it vates different kinase enzymes belonging to the MAPK family. stimulates calmodulin-like proteins that interact with Ca ions. The phosphorylation cascade is therefore thought to be involved Changing their conformation in response to Ca binding, calm- in Cd signaling to the nucleus (Fig. 1A). odulin proteins regulate a variety of mechanisms, including ion Calcium ions and calmodulin are well-known second messen- transport, gene regulation, metabolism and stress tolerance that gers of external stimuli, and the participation of this system in coordinate, at least in part, the plant response to Cd. The Ca/ 664 Plant Signaling & Behavior Volume 5 Issue 6 calmodulin system is also involved in sensing other heavy metals, Cd ions is rather slower than to Cu. This could be due to the fact and in fact, transgenic plants expressing a tobacco calmodulin-like that Cd stimulates an oxidative stress as a secondary effect, which protein exhibit increased Ni tolerance and Pb accumulation. is responsible for the MAPKs activation, delaying the phospho- Another mechanism that is thought to be involved in Cd sens- rylation cascade. ing is the reduced glutathione-oxidized glutathione ratio (GSH/ Summarizing, heavy metal stress signals appear to be trans- GSSG). Glutathione can control the differential expression of duced through a variety of pathways that overlap and cross-talk. antioxidant enzymes, such as chalcone synthase, phenylalanine Activation of phosphorylation cascades, Ca-calmodulin system, ammonia lyase, superoxide dismutase or glutathione reductase, ROS signaling and stress-related hormones eventually converge usually induced by heav y metal stress. During Cd stress, a reduc- regulating transcription factors that are deputed to the activation tion in GSH/GSSG ratio has been observed in different plant of gene sets responsible for response to stress (Fig. 1A). species, with the consequent activation of the response genes. Modulation of transcription factors. Transcriptomic changes Regulation in hormone synthesis has also been observed dur- upon Cd stress have been investigated in several plant species, 29,30 24 31 ing heavy metal stress. Treatments with Cd or Cu, for instance, including Arabidopsis, pea and barley. This analysis led enhance jasmonic acid content in Arabidopsis, Oryza and bean. to the identification of numerous transcription factors (TFs), 32-34 Ethylene synthesis is also increased upon treatment with Cd, Cu, involved in Cd plant response. Fe, Zn, and in the case of Cd and Cu, this increase is due to an Cd-responsive TFs share the same signal transduction path- upregulation of ACC synthase transcription and enhanced activ- way with other stress-related TFs, and can therefore be acti- ity. Salicylic acid (SA) is another well-known hormone involved vated by other abiotic stresses such as cold, dehydration, SA and in stress signaling in plants and exposure to Cd has been shown H O . Moreover, the modulation of TFs belonging to several 2 2 to stimulate SA accumulation in roots. All these data together families demonstrates the complexity of the response of plants to 32 36 suggest that cross-talk exists between heavy metal signaling and Cd stress. TFs belonging to different families, such as WRK Y, 37 38 biotic stress signaling. It has been shown that a mild exposure basic leucine Zipper (bZIP), ethylene-responsive factor (ERF) to heavy metals can induce greater plant resistance against viral and myeloblastosis protein (MYB) play a significant role in and fungal infections without being connected to the direct toxic controlling the expression of specific stress-related genes after Cd effect of the metal. Conversely, application of SA on barley seed- treatment. lings before Cd treatment caused partial protection against the Cd regulates the expression of ERF proteins (e.g., ERF1 and 25 30 heavy metal toxicity. ERF2, ) belonging to the APETALA2 (AP2)/ethylene-respon- Hormone signaling is not the only example of redundancy sive-element-binding protein (EREBP) family and is also able to between heavy metal and (a)biotic stress. The signal mediated by bind to several pathogenesis-related promoters and dehydration Reactive Oxygen Species (ROS) is also reported. In fact, heavy responsive elements (DRE). An example of TF induced by Cd metal stress triggers the accumulation of ROS both directly, via and binding to DR E motif is DR EB2A: it can specifically interact Fenton or Haber-Weiss reaction and indirectly, unbalancing the with the promoter region of the Rd29A (desiccation responsive) activity of antioxidative enzymes, as in the case of Cd. H O gene, on the DRE motif, inducing the transcription of Rd29A 2 2 plays a role as signal molecule inducing defense mechanisms after Cd-exposure. against both abiotic stresses, such as temperature and ozone, In addition, it was observed that MYB4 is highly expressed 27 34 and pathogen attack. Based on the evidence that both heavy after Cd and Zn treatment in A. thaliana, while MYB43, metal stress and ROS-mediated biotic stress induce phytoalex- MYB48 and MYB124 proteins are specifically induced by Cd in ins biosynthesis, it has been hypothesized that heavy metal and roots. Furthermore, the TFs MYB72 and bHLH100 (belong- biotic stress response share common signals. It remains anyway ing to the helix-loop-helix TFs group) were studied for their doubtful whether the effects of heavy metals on plants should be implication in metal homeostasis because they showed an altered attributed to their direct effect on membranes, cellular enzymes expression after Cd exposure. In Cd-treated Thlaspi caerulescens 34,36 and photosynthetic apparatus or to their indirect effect caused by MYB28 and WRKY53 are strongly expressed, even if the lat- the induction of some signaling pathways that are responsible for ter has been supposed to be involved in the signal transduction the so called heavy-metal stress response. pathway regulating the activity of other TFs. It is noteworthy that plant cells probably transduce heavy OBF5, belonging to the bZIP group, regulates the expression metal signaling in different ways for different heavy metals. The of glutathione S-transferase binding to its promoter region in a main differentiation is probably due to the fact that some metals Cd-induced manner. TGA3 protein also has a putative role in do not have any known function and could induce deleterious modulating gene expression upon Cd-treatment, as well as in effects even at low concentration. Conversely, other metal ions response to biotic stress. Recently, BjCdR15, orthologous to take part in the normal cell metabolism and are shown to be toxic TGA3, has been identified in B. juncea after short Cd treatment; only at high concentrations. A good example of this is the activa- BjCdR15 inu fl ences the expression of several metal transporters, tion of the phosphorylation cascade of MAPK proteins induced being therefore involved in long distance root-to-shoot Cd trans- 7,32 by Cu and Cd. Cu stress rapidly activates SIMK, MMK2, port. In addition, its overexpression in A. thaliana and tobacco MMK3 and SAMK kinases, and their activation is probably enhances Cd tolerance and accumulation in shoots. 19 40 the consequence of oxidative stress generated by the metal ion. Finally, other TFs named metal-responsive TFs (MTFs), Conversely, activation of the above-cited MAPKs in response to control the expression of metallothioneins by binding metal- www.landesbioscience.com Plant Signaling & Behavior 665 41 regulatory elements (MREs) in their promoter region. MTF-1, and Cd ions are bound to the thiolic groups of Cys. Cd-PCs com- for instance, was first identified as a Zn dependent MR E-binding plexes are transported into the vacuoles where they pack to form 42 8,51 factor essential for Zn and Cd dependent induction of the high-molecular-weight complexes (Fig. 1B). PCs also play a murine MT-I and MT-II genes. role in long-distance Cd transport from root to shoot: this would Activation of metal transporters. Once Cd has entered the contribute towards keeping Cd accumulation low in the root, cells, plants use various strategies to cope with its toxicity. One causing extra Cd transport to the shoot. such strategy consists of transporting Cd out of the cell or seques- Genes encoding PCS have been cloned from different organ- tering it into the vacuole, thereby removing it from the cytosol. isms, for example, OsPCS1, TaPCS1, AtPCS1 and CePCS1 Members of different transporter families contribute to Cd resis- from rice, wheat, Arabidopsis and Caenorhabditis elegans respec- 8,56,57 tance. The ABC transporter AtPDR8 has been shown to medi- tively, and BjPCS1 from the metal-tolerant plant Brassica ate Cd extrusion out of the plasma membrane of root epidermal juncea. Experimental data confirmed that accumulation and cells. Detoxification of Cd is also achieved by members of the tolerance to Cd is increased in transgenic plants overexpress- ZIP (ZRT, IRT-like protein) family. They are plasma-membrane ing PCS. In B. juncea, enhanced tolerance to Cd, As and Zn proteins induced in roots and shoots of Arabidopsis in response to was associated to the overexpression of AtPCS. However, an Zn-limiting conditions, and being involved in the xylem upload- excessive expression of AtPCS caused hypersensitivity to Cd in ing process, are potentially implicated in Cd root-to-shoot trans- Arabidopsis plants. port. IRT1 is essential for root iron uptake in response to iron Fina lly, meta llothioneins (MTs) are low-molecular-weight Cys- deficiency but it also accepts Cd as a substrate. HMA4, a mem- rich peptides also able to bind metal ions, such as Cd. Differently ber of the P-type metal ATPase, functions as Zn/Cd transporter from PCs, MTs are products of mRNA translation, induced in and by loading Cd into the xylem, it increases translocation to response to heavy metal stress. Binding to Cd, MTs also con- 47,48 the shoot where Cd might have less damaging effects. Another tribute to detoxifying the cytosolic environment from Cd toxic- family of metal transporters implicated in the mobilization of ity (Fig. 1B). Indeed, it has been reported that overexpression of Cd is the NRAMP (natural resistance-associated macrophage mouse MT in tobacco plants enhances Cd tolerance in vitro, protein). Indeed, expression of AtNRAMP1, AtNRAMP3 and whereas the Arabidopsis MT2a and MT3 increased Cd tolerance AtNR AMP4 in yeast showed that these proteins are able to trans- when expressed in Vicia faba. Moreover, B. juncea MT2 confers 49 64 port Cd. Recently, it was suggested that AtNR AMP6 functions increased tolerance to Cd and Cu in transgenic A. thaliana. In inside the cell either by mobilizing Cd from its storage compart- a recent study on hybrid Populus, it was shown that high levels of ment or by taking up Cd into a cellular compartment where it is MT2b correlated with Cd and Zn concentrations, demonstrating toxic. Finally, transporters of the CDF (cation diffusion facilita- that increased MT2b expression is one of the plant responses to tor) family appear to mediate the cytoplasmic efu fl x and vacuolar chronic metal exposure. sequestration of divalent metal cations such as Zn, Cd, Co, Ni or Mn. Conclusions and Perspectives Biosynthesis of chelating compounds. In the cell, Cd is che- lated by thiol-containing ligands such as glutathione (GSH) Heavy metal pollution is a significant environmental problem and its derivative phytochelatins (PCs), to allow the transport that is nowadays being evaluated as a major threat to humans. of Cd-complexes into the vacuole or in the apoplast by ATP- Researchers are concerned in developing new technologies for low dependent membrane pumps. GSH is required for PCs syn- cost and environmentally friendly land reclamation techniques. thesis. This process is catalyzed by the cytosolic PCs synthetase Increasing our knowledge about the mechanisms that enable (PCS). It has been shown that PCS is constitutively expressed, plants to cope with heavy metal stress would help in creating new but post-translationally activated by heavy metals. A recent tools applicable in phytoremediation, which is any technology study confirms that PCS is regulated by a Cd-dependent phos - that uses plants to reclaim polluted soils and waters. It is therefore phorylation on a Thr residue next to the catalytic site, and it of primary importance to further dissect the processes of heavy could therefore function as a “Cd sensor”. PCs have the gen- metal detoxification and signaling pathways in plants, to identify eral structure (γ-Glu-Cys)n-X (where n is a variable number from useful targets for biotechnological applications to increase plant 2 to 11 and X an amino acid such as Gly, β-Ala, Ser, Glu or Gln) t fi ness in heavy metal polluted sites. 4. Buchet JP, Lauwerys R, Roels H, Bernard A, Bruaux P, 8. Clemens S. 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