Abstract
Heavy metals are required by plants in trace amounts for adequate growth and development, and their absence may lead to several detrimental effects during plant growth and development. Among them, one of the imperative trace elements required by plants for normal growth and development is copper. Copper (Cu) also serves as an important cofactor of many proteins. However, the details regarding these many Cu proteins are certainly limited. Nonetheless, the role played by these Cu proteins is of paramount significance. Cu holds an indispensable position in this regard; nevertheless, if its amount surpasses the required limit, it can lead to serious repercussions. Therefore, in order to maintain such a delicate balance, there exists an innate system within plants, which controls its absorption, distribution, and excretion within plants. There exists a unique set of proteins within plants termed as transport proteins, which regulate this delicate balance within plants. In the upcoming discussion, three of the most significant transport proteins also known as transporters are brought to light. These transport proteins include P type ATPases, that are responsible for the transport of Cu ions across the cell membrane, COPT proteins, that are responsible for the transport of Cu ions to various different cellular compartments, and chaperones that do not actually contain Cu but work like others, which are possessed with Cu. NRamp family gene analysis in soyabean seedlings also revealed their role during Cu and other heavy metal strain. The expression of this gene family also gets altered during heavy metal toxicity. The role of SPL7 transcription factor, in Cu homeostasis, has also been highlighted. In addition to it, the related role of Cu transport systems in biosynthesis and homeostasis has also been discussed.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
13.1 Introduction
Plants, in addition to light and water, also require certain metal elements, in small amounts, which ensure apposite growth and development. Such elements are obtained either from the soil or from foliar applications (Yruela 2009). To draw these elements from soil in highly calculated way, plants have undergone evolution and, as a consequence of it, have evolved structures and ways to get to these mineral elements and also to ensure its efficient distribution. Presently, 17 elements are regarded by biologists as essential. Depending upon their required concentration, they are termed as micronutrients or macronutrients. If the required concentration of the mineral is below 100 mg/kg DW, the required minerals will be categorized as micronutrients, and if the required concentration of the mineral is above 1000 mg/kg DW, they are termed as macronutrients (Printz et al. 2016). To make it possible, plants have successfully evolved an in-built set of transporter proteins, channels, and pumps. These innate devices within plants help plant to not only absorb but also transfer and distribute minerals as per requirements. In reduced suitability of Fe during various physiological developmental stages, Cu serves as a strong alternative (Burkhead et al. 2009). In general, Cu occurrence is 60 mg/kg, and in European environment, its range is between 11.4 and 17 mg/kg (Alloway 2013).
Copper (Cu) is a vital element—a micronutrient, which is required by plants in minuscule amounts, for its proper growth and development. It is an important transition metal active in redox reaction, which carries many plants physiological processes as it can present in several oxidation states (Yruela 2005). The major functions performed by copper include its contribution in electron transport chain vital for both linked with photosynthesis and respiration. It also aids plants in sensing ethylene, metabolism occurring in cell wall, protection against oxidative stress, and synthesis of molybdenum cofactor (Yruela 2009). The significance of copper in plants’ life cannot be overlooked.
Nevertheless, if the amount of Cu exceeds compared to the bare minimum of it being required, it can lead to plant damage and deterioration. It not only hampers the regular plant growth but also negatively affects the regular cellular processes occurring in the cells. Several studies have mentioned the negative effects as a result of excessive amounts of Cu on plant germination and growth, photosynthetic activity, and antioxidant response in case of several agricultural crops. The inhibition of mineral nutrition, biosynthesis of chlorophyll, and activity of antioxidant enzymes have been proved (Mir et al. 2021). Therefore, it can cause both damage and deterioration simultaneously. Such an increased concentration of Cu in the soil leading to higher levels of toxicity may occur when Cu becomes rich in parental materials, and pH of soil promotes metal availability, or soil pollution occurs by mining activities and waste deposits, or through intensive usage of plant disease control Cu-containing chemicals in agricultural, or rigorous use of manure or sewage sludge (Rehman et al. 2019; Kumar et al. 2021). For most of the crops, the serious toxicity level is over 20–30 mg/kg leaf dry weight, whereas in metallophytes tolerant to Cu, leaves may possess around 1000 μg/g leaf dry weight (Kupper et al. 2009; Monni et al. 2000).
However, as mentioned earlier, its absence can also have negative effects on growth and development of plants. The dearth of copper causes alterations in the expression of genes and also exhibit several deficiency symptoms in plant parts such as leave structure that gets distorted. The leaves first turn yellow, which can even lead to tissue death (Marschner 1995). Hence, its appropriate amount is required by plants to ensure proper growth and development. This indicates that, in plants, there exists a well-established mechanism of metal uptake by the roots from the soil and also for its translocation and distribution in all the required parts of plants. The maintenance of their concentration in the cytosol is indispensable for normal plant growth and development. To regulate these complicated and intricate processes, different transport proteins present within plants play their role.
Biochemical and molecular techniques have already helped scientists to understand these processes and will help further to explore ways to grow plants in heavy metal-contaminated zones, by developing varieties of plants, which will not absorb Cu heavy metals beyond requirement or will be able to get hold on them by developing in them both efficient and effective efflux, compartmentalization, or detoxification mechanism in response to its absorption besides requirement. Phytoremediation gained momentum to deal with the issue of soil contaminated with heavy metal (Salt et al. 1998). In the upcoming section, the transport mechanism of this indispensable metal in plants will be elucidated.
13.2 Mechanism of Copper (Cu) Transport in Plants
The importance of copper (Cu) in plants cannot be denied, however its excess can have repercussions is an established fact too. This suggests that there exists an in-built machinery that regulates the adequate transport of copper in plants. This further suggests that the device present in it is both delicate and sophisticated, which ensures regulated transport of copper in plants. However, the research on it was really limited, until research was conducted in which the transport processes in yeast and various other eukaryotic organisms were published (Nevo and Nelson 2006).
Under physiological circumstances, Cu exists in two forms, the reduced and oxidized Cu states as Cu I and Cu II, respectively. This dual nature helps it to bind with a variety of substrates (Cohu and Pilon 2010). This dual nature facilitates it to make bonds with diverse group of molecules prominently proteins, not only to run biochemical reactions but also to maintain structural ensembles (Festa and Thiele 2011). Nevertheless, redox Cu has the potential to produce reactive oxygen species (ROS) via a popular method called Fenton reaction, thereby damaging the proteins, DNA, and other biological molecules (Hänsch and Mendel 2009).
Cu homeostasis in plants is mediated by SPL7, Cu-responsive transcription factor. This SPL7 is regarded as a functional homolog of Cu response regulator 1 (CR1), which has semblance with SBP domain transcription factor that has been found in signaling of Cu in Chlamydomonas reinhardtii (Yamasaki et al. 2004; Kropat et al. 2005; Sommer et al. 2010). These SBP domains appear to be highly conserved domains for DNA binding and able to identify the TNCGTACAA site and particularly the GTAC core sequence (Printz et al. 2016). In plants, direct interaction between Cu and SPL7 is still not evident. However, it has been hypothesized that under sufficient Cu conditions, SPL7 may attach with Cu via specific Cu-complexes interactions, and this results in the lack of SPL7 ability to join the GTAC motif in the promotor of target genes (Garcia-Molina et al. 2014). This significant aspect of SPL7 regulation of Cu homeostasis needs further research. The research studies exhibited that there are several components, which are responsible for both efficient and effective Cu transport machinery. The different components of Cu transport machinery will be discussed in this chapter.
13.3 P-Type ATPase Copper Transporters
P-type ATPases have been reported in various different organisms that are meant to transport heavy metals across the plasma membrane. These heavy metals are both beneficial and harmful for plants, and this is basically dependent on the amount of it being present in the plant cell. P-type ATPases are a large superfamily that has subgroups in it. Subgroups make use of ATP to pump a large number of substrates carrying charge across various biological membranes and are differentiated on the basis of phosphorylated intermediate during the reaction process. Based on the type of substrate, P-type ATPase transport, they are sorted into five groups.
CPx ATPases belong to P-type ATPases, which have been associated with heavy metal transportation across the cell membrane (Solioz and Vulpe 1996). CPx ATPases are not only responsible for the absorption of heavy metal in the plants but also prevent the accumulation of heavy metals to deleterious extent. In human Menkes disorder, the gene encodes a defected copper pump, which results in the accumulation of copper to toxic levels. CPx ATPases are generally linked with Cu and Cd translocation; nevertheless, in E. coli and Synechocystis PCC 6803, they have been linked with Zn translocation too (Beard et al. 1997).
Copper (Cu) is a metal that holds a unique position, as far as its role in plants is considered. It is both a blessing and a menace for a cell, and the only thing that matters is its amount. Therefore, to maintain such a delicate balance, several constituents play their part. P-type ATPase copper transporters, which are homologous to human and yeast genes, have been reported to regulate the transport of copper across the endomembrane system in Arabidopsis (Hirayama et al. 1999; Woeste and Kieber 2000). Burkhead et al. (2009) stated that heavy metal transferring P-type ATPases (HMAs) five to eight are found to be related to Cu homeostasis. Nevertheless, HMA 5 among all four of them has been greatly linked with outflow of Cu and vascular translocation. It has been found in inordinate amounts in both plant roots and flowers and are significantly increased, when plethora of Cu gets accumulated in these plant parts (Andrés-Colás et al. 2006).
According to Axelsen and Palmgren (2001), three other putative Cu-translocating genes have been recognized; however, their mode of action has not been eloquently described. Cu transfer to chloroplast is also vital as it serves as a cofactor for stromal enzyme copper/zinc superoxide dismutase (Cu/Zn SOD) and for thylakoid lumen protein, which plays role in ETC initiating in cytochrome B6f complex and culminating in photosystem I. In this transfer of Cu to chloroplast, the role of P-type ATPase Cu transporter cannot be discounted (Shikanai et al. 2003).
13.4 COPT Copper Transporters
The dual nature of Cu has led the plants and other organisms to develop an advanced homeostatic network in order to control uptake, transfer, utilization, and detoxification/export of Cu (Himelblau and Amasino 2000; Clemens 2001). The Cu homeostasis involves a main step regarding the uptake of Cu via cell membrane, and for mediation of its uptake, different forms of transporter proteins have been reported. Among these, the main group is the COPT (COPper transporter)/Ctr (Copper transporter) proteins belonging to several protein families in diverse organisms (Puig and Thiele 2002). Another transporter type for Cu movement from cytosol into organelles in plants and humans is P-type adenosine triphosphate pump (Williams et al. 2000; Williams and Mills 2005). In few studies, it has also been documented that other metal transporters can also carry Cu into the cells. For example, in Arabidopsis, two transporters of OPT/YSL Fe transporter family, namely, YSL1 and YSL3, can carry Cu from plant leaves to seeds (Waters et al. 2006). Similarly, ZIP2 and ZIP4 belonging to ZIP Zn transporter family transport Cu (Puig et al. 2007a, b).
The role of COPT/Ctr proteins in Cu uptake has been described principally in yeast, Saccharomyces cerevisiae (Dancis et al. 1994). Later, COPT/Ctr proteins transporting Cu were characterized in diverse organisms, for instance, in the case of plants: AtCOPT1, AtCOPT2, AtCOPT3, AtCOPT4, and AtCOPT5 in Arabidopsis (Sancenon et al. 2004) and OsCOPT1 and OsCOPT5 in rice (Yuan et al. 2010). In rice, the COPT family is composed of seven members, COPT1 to COPT7. Among these, COPT1 and COPT5 are able to develop homodimers or a heterodimer. Both of these COPTs can bind to multiple sites of XA13 protein in rice, which is considered as a susceptible protein to plant pathogenic bacterium Xanthomonas oryzae pv. oryzae (Xoo) (Yuan et al. 2010). Except the two COPTs, namely, COPT1 and COPT5, the rest of COPTs have been described to function individually or jointly to carry Cu transport in distinctive rice tissues (Yuan et al. 2011).
Copper (Cu+2) gets reduced to Cu+, in order to be carried by COPT transporters. The COPT family comprises of six constituents, among which COPT1, COPT2, and COPT6 exist on plasma membrane and COPT3 and COPT5 in internal membranes. Cu uptake by COPT proteins is an important phenomenon and has been studied by comparable yeast mutants (Sanz et al. 2019). Seven member COPT-type gene families are found in rice plant, one of the major crop plants found in the world (Yuan et al. 2011). COPT proteins have been reported in transfer of Cu in many major parts of plants. Puig (2014) reviewed and stated that COPT1 plays role in absorption of Cu in plant roots, COPT6 plays role in the distribution of Cu in plant shoots, and COPT5 activates and organizes Cu from organelles meant for storage. Therefore, in the light of aforementioned functions of COPT proteins, it can be stated that the COPT proteins play an indispensable role in Cu homeostasis in plant. COPT regulates Cu, which has a role in Arabidopsis circadian clock. Sancenon et al. (2004) reported that during the period of Cu shortage, COPT1 in SPL7-dependent fashion gets activated, which ensures efficient absorption of Cu from a culture medium. Perea-García et al. (2013) reported, that in response to Cu scarcity, expression enhances manifold in SPL7-dependent manner. Furthermore, the expression of two transport proteins of ZIP family, ZIP2 and ZIP4, that mediate the transport of divalent cations is regulated by the presence of Cu (Wintz et al. 2003; Del Pozo et al. 2010).
13.5 Copper Chaperones
Copper chaperone found in plants is similar to the one found in all eukaryotic organisms, which has been revealed by complementation studies conducted in S. cerevisiae (Koch et al. 1997; Peña et al. 1999). These are proteins that do not possess Cu but perform job similar to the proteins containing Cu (Andrés-Colás et al. 2006). It is vital to maintain the levels of Cu within plant cells. These are actually a set of soluble proteins, which possess a special domain that is meant to bind Cu. Thus, their Cu-chelating potential helps them to both efficiently and effectively regulate Cu homeostasis within plant cell (Shin et al. 2012) to evade copper-induced harmful effects. Moreover, Cu chaperones carry out delivery of Cu to particular Cu proteins and compartments. Brewer (2010) highlighted the significance of maintaining Cu within plant cells, and if the levels of free Cu go unchecked, it generated super oxide and hydrogen peroxide reactive oxygen species, and hydroxyl radicals negatively affect proteins, lipids, and DNA of the cells. In order to avoid the levels of free Cu within a cell, it needs to be chelated within it. This guarantees efficient and effective transfer and homeostasis.
In the case of Arabidopsis, its genome encodes seven Cu chaperones, namely, Cu chaperone for superoxide dismutase (CCS), antioxidant protein1 (ATX1), ATX1-like Cu chaperone (CCH), cytochrome c oxidase 11 (COX11), COX17, and two homologs of the yeast Cu chaperone (HCC1 and HCC2) (Puig et al. 2007a, b; Burkhead et al. 2009; Attallah et al. 2011). CCS carries Cu to Cu/Zn superoxide dismutases (SODs) in the chloroplast, cytoplasm, and peroxisome (Burkhead et al. 2009). ATX1 and CCH exhibit maximum sequential homology with the yeast protein (ATX1), and both of these can complement the yeast ATX1 mutant; however, they possess diverse properties and roles in Cu homeostasis (Shin et al. 2012). ATX1 enhances tolerance against Cu excess as well as deficiency through its Cu-binding MXCXXC motif (Shin and Yeh 2012; Shin et al. 2012. Additionally, Cu chaperones COX11, COX17, HCC1, and HCC2 function in mitochondrial respiration (Attallah et al. 2011). While extensive studies have been conducted on Cu chaperones, considerable information is still missing, specifically involving whether Cu chaperones and Cu are transported into the nucleus and induce plant defense responses.
13.6 Natural Resistance-Associated Macrophage Protein (NRAMP)
The NRAMP genes have been widely reported in organisms ranging from bacteria to yeast, including plants, mice, and human beings. This gene family has been widely found in the transport of heavy metal divalent ions across the plasma membrane (Nevo and Nelson 2006). In plants, numerous members of this gene family have also been reported, and their functions have been characterized. For example, in the case of Arabidopsis, six NRAMP proteins have been demonstrated (Mäser et al. 2001). Among these proteins, AtNRAMP1 is responsible for regulating Fe homoeostasis (Curie et al. 2000), and as a high-affinity transporter, it is involved in the uptake of Mn (Cailliatte et al. 2010). The two proteins, namely, AtNRAMP3 and AtNRAMP4, exist on the vacuolar membrane, and during the phase of seed germination, both perform mobilization of vacuolar Fe (Lanquar et al. 2005). AtNRAMP6 is directed to endomembrane compartment, which is vesicular-shaped, and this protein works as a metal transporter intracellularly with known association with Cd tolerance (Cailliatte et al. 2009).
In rice, it has been reported that three NRAMP proteins take part in Fe, Mn, and Cd uptake (Takahashi et al. 2011; Sasaki et al. 2012; Yang et al. 2014), whereas OsNrat1 participates in the uptake of Al from tip cell walls of roots into the cell, which creates Al tolerance in rice (Li et al. 2014). Likewise, in legumes, many NRAMP genes have been detected. For example, AhNRAMP1, a NRAMP gene from peanut, has been shown that it is considerably induced by Fe deficiency in leaves and roots, and this gene, when heterologously expressed in tobacco, results in accumulation of Fe in young plant leaves and Fe deprivation tolerance (Xiong et al. 2012). Additionally, gene MtNRAMP1 is specifically restricted to the plasma membrane in case of a model legume named Medicago truncatula, and this gene shows highest expression levels in roots and nodules, depicting its major involvement as a transporter in apoplastic uptake of Fe in rhizobia-infected cells (Tejada-Jiménez et al. 2015).
In soyabean studies, it has been revealed that the gene regulation gets affected by the shortage of N, P, K, Fe, and S. Additionally, the regulation gets affected by the buildup of Fe, Cu, Cd, and Mn. This suggests that Gm NRAMP genes play role in various different stress-related pathways and perhaps are involved in cross talk in nutrient stress pathways (Illing et al. 2012). In order to study the Gm NRAMP responses during heavy metal stresses, expression of these genes was calculated, by exposing soyabean seedlings to plethora of Fe, Cu, Cd, and Mn. In this study, only 10NRAMP gene expression was noticeable. Under excess Cu, GmNRAMP5a expression was enhanced in both leaves and roots, and expression of GmNRAMP1a was amplified in roots; however, the expression of GmNRAMP2a was diminished in both leaves and roots, respectively. Nevertheless, two NRAMP genes exhibited a unique, rather conflicting drift in soyabean leaves and roots, in response to inordinate concentration of Cu (Qin et al. 2017).
13.7 Relating the Biosynthetic and Homeostatic Roles of Cu Transport Systems
Cu serves as a cofactor, and thus, it can be contended that all the Cu transport proteins have some role in biosynthesis of different products (Burkhead et al. 2009). One of the biosynthetic functions can be viewed in the context of three ATP-driven pumps, namely, HMA6, HMA7, and HMA8. On the other hand, homeostatic function of the transport protein can be viewed in the context of regulating apposite concentrations of Cu in different compartments both locally and widely in different plants, which can be noted over a period of time. This appears to be one of the main roles played by the members of COPT family. COPT1 and COPT5 phenotypes are found where Cu concentrations are comparatively low and are evident in tissues, where transport proteins are generally expressed; however, this cannot be explained by the absence of Cu enzyme function, and this can only be explained in terms of Cu/Zn superoxide dismutase, which stops its function at once Cu shortfall happens. This decrease in the concentration of Cu/Zn superoxide dismutase follows the increase in miR398 through SPL7 (Yamasaki et al. 2007, 2009), which is among one of the four Cu-associated RNAs (Burkhead et al. 2009). Besides other functions, it was documented that Cu micro RNAs regulate the plethora of Cu in order for it to be available as cofactor where and when needed by the Cu proteins (Burkhead et al. 2009).
Cu homeostasis in plants is controlled by the SPL7 (squamosa promoter binding protein-like) transcription factor, which is active during Cu deficiency (Yamasaki et al. 2007; Bernal et al. 2012). In case of Arabidopsis, major targets of SPL7 include the genes COPT1, COPT5, and COPT6. COPT1 is engaged in encoding high-affinity Cu transporter of the roots, which is involved in primary Cu uptake (Sancenon et al. 2004). COPT6 gene has been shown to express in shoots and is found in the plasma membrane (Jung et al. 2012). Both genes are upregulated in plants during Cu deficiency so as to enhance the absorption capability at a systemic level (COPT1) and much precisely in photosynthetic plant cells (COPT6) (Sancenon et al. 2004; Jung et al. 2012). COPT5 gene is also expressed under Cu deficiency conditions, and it carries Cu efflux from the vacuole, demonstrating its role in Cu remobilization (Klaumann et al. 2011). It has been shown that Cu binds very firmly to its targets (Lippard and Berg 1994), and consequently, any competing Cu-utilizing proteins must be removed when Cu becomes deficient to permit the favored delivery of Cu to plastocyanin. This mechanism in plants regarding “copper economy” encompasses the posttranscriptional regulation of dispensable Cu enzymes by several microRNAs, which are in turn controlled by SPL7 (Yamasaki et al. 2007). The transcripts that encode the vital Cu proteins like plastocyanin are not directed for degradation by the microRNAs (Abdel-Ghany and Pilon 2008), which suggests that such proteins are important targets for deficient Cu.
13.8 Conclusion
Copper (Cu) is a vital element, and its requirement by plants as a micronutrient, as a transporter, and as a cofactor has not been elucidated thoroughly. Nonetheless, research has been conducted in the past and is still being continued on the functions of Cu in plants. As a result of these research efforts, it has been revealed that as a micronutrient, it is required by the plants in miniscule amounts; nevertheless, it is imperative for plant growth and development. In addition to it, the role of Cu as a cofactor cannot be discounted. The role of copper as Cu proteins is sine qua non for the normal functioning of plant proteins. In the light of discussion, it can be concluded that it is sine qua non for plant’s survival; however, it should always be understood that it is required by the plants in very low amounts, and if it exceeds the limit, it can prove detrimental to plant growth and development and can even threaten its very existence. Therefore, in order to maintain such a delicate balance, plant has developed an efficient as well as an effective metal transport system, in which several players play their role to regulate the concentrations of different metals like copper in them.
Copper (Cu) homeostasis in plants is mediated by SPL7 regulator, which is the functional homolog of copper response regulator (CRR1), which has some semblance with the one reported in Chlamydomonas reinhardtii. To maintain the levels of Cu in plants, different transport proteins play their part. The major and the most important proteins among them include P-type ATPase copper transport proteins, which regulate movement of copper across the plasma membrane. P-type ATPase is not only responsible for the uptake of Cu in plants but also prevents its inordinate accumulation that can lead to deleterious consequences. Additionally, COPT transporters exist in plants, a six-member family, in which COPT1, COPT2, and COPT6 are located on cell membrane and COPT 3 and COPT5 are located on internal membranes. These are responsible for transport of Cu to various different parts of plants. The role of Cu chaperones, one being without Cu, is similar to the one with Cu. These too play role in the regulation of Cu within plant cells. The expression of NRamp genes also gets altered during heavy metal toxicity in plants, when studied in soyabean seedlings.
Cu transport systems have a linked function in two most significant activities occurring within a cell, that is, biosynthesis and homeostasis. Biosynthetic role can be explained in terms of three ATP-driven pumps, namely, HMA6, HMA7, and HMA8. Homeostatic role can be explained in terms of regulating apposite concentration of Cu to be made available to proteins as per requirement. Nevertheless, this hypothetical statement needs to be proven in future. To sum up, more extensive research studies are suggested to enhance our understanding of Cu homeostasis within plants. Nonetheless, as yet, we can say that Cu transport is a complex phenomenon, which is overseen by an intricate machinery built within plants.
Abbreviations
- ATP:
-
Adenosine triphosphate
- Cu:
-
Copper
- CR:
-
Copper response regulator
- N ramp:
-
Natural resistance-associated macrophage protein
- ROS:
-
Reactive oxygen species
References
Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283:15932–15945
Alloway BJ (2013) Sources of heavy metals and metalloids in soils. In: Alloway BJ (ed) Heavy metals in soils environmental pollution. Springer, Dordrecht, pp 11–50
Andrés-Colás N, Sancenón V, Rodríguez-Navarro S, Mayo S, Thiele DJ, Ecker JR et al (2006) The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. Plant J 45:225–236
Attallah CV, Welchen E, Martin AP, Spinelli SV, Bonnard G, Palatnik JF, Gonzalez DH (2011) Plants contain two SCO proteins that are differentially involved in cytochrome c oxidase function and copper and redox homeostasis. J Exp Bot 62:4281–4294
Axelsen KB, Palmgren MG (2001) Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiol 126:696–706
Beard SJ, Hashim R, Membrillo-Hernandez J, Hughes MW, Poole RK (1997) Zinc (II) tolerance in Escherichia coli K-12: evidence that the zntA gene (o732) encodes a cation transport ATPase. Mol Microbiol 25:883–891
Bernal M, Casero D, Singh V, Wilson GT, Grande A, Yang H, Dodani SC, Pellegrini M, Huijser P, Connolly EL (2012) Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/FRO5 and the copper dependence of iron homeostasis in Arabidopsis. Plant Cell 24:738–761
Brewer GJ (2010) Copper toxicity in the general population. Clin Neurophysiol 121:459–460
Burkhead JL, Reynolds KA, Abdel-Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816
Cailliatte R, Lapeyre B, Briat JF, Mari S, Curie C (2009) The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem J 422:217–228. https://doi.org/10.1042/BJ20090655
Cailliatte R, Schikora A, Briat J-F, Mari S, Curie C (2010) High-affinity manganese uptake by the metal transporter NRAMP1 is essential for arabidopsis growth in low manganese conditions. Plant Cell 22:904–917. https://doi.org/10.1105/tpc.109.073023
Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486. https://doi.org/10.1007/s004250000458
Cohu CM, Pilon M (2010) Cell biology of copper. In: Rüdiger H, Mendel R-R (eds) Cell biology of metals and nutrients plant cell monographs. Springer, Heidelberg, pp 55–74
Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347:749–755. https://doi.org/10.1042/bj3470749
Dancis A, Yuan DS, Haile D, Askwith C, Eide D, Moehle C, Kaplan J, Klausner RD (1994) Molecular characterization of a copper transport protein in S. cerevisiae: an unexpected role for copper in iron transport. Cell 76:393–402. https://doi.org/10.1016/0092-8674(94)90345-X
Del Pozo T, Cambiazo V, González M (2010) Gene expression profiling analysis of copper homeostasis in Arabidopsis thaliana. Biochem Biophys Res Commun 393:248–252
Festa RA, Thiele DJ (2011) Copper: an essential metal in biology. Curr Biol 21:R877–R883
Garcia-Molina A, Xing S, Huijser P (2014) Functional characterisation of Arabidopsis SPL7 conserved protein domains suggests novel regulatory mechanisms in the Cu deficiency response. BMC Plant Biol 14:231. https://doi.org/10.1186/s12870-014-0231-5
Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266
Himelblau E, Amasino RM (2000) Delivering copper within plant cells. Curr Opin Plant Biol 3:205–210
Hirayama T, Kieber JJ, Hirayama N, Kogan M, Guzman P, Nourizadeh S, Alonso JM, Dailey WP, Dancis A, Ecker JR (1999) Responsive-to-antagonist1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97:383–393
Illing AC, Shawki A, Cunningham CL, Mackenzie B (2012) Substrate profile and metal-ion selectivity of human divalent metal-ion transporter-1. J Biol Chem 287:30485–30496
Jung HI, Gayomba SR, Rutzke MA, Craft E, Kochian LV, Vatamaniuk OK (2012) COPT6 is a plasma membrane transporter that functions in copper homeostasis in arabidopsis and is a novel target of SQUAMOSA promoter binding protein-like 7. J Biol Chem 287:33252–33267
Klaumann S, Nickolaus SD, Fürst SH, Starck S, Schneider S, Ekkehard NH, Trentmann O (2011) The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocation of copper in Arabidopsis thaliana. New Phytol 192:393–404
Koch KA, Peña MMO, Thiele DJ (1997) Copper-binding motifs in catalysis, transport, detoxification and signaling. Chem. & . Biol 4:549–560
Kropat J, Tottey S, Birkenbihl RP, Depège N, Huijser P, Merchant S (2005) A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proc Natl Acad Sci U S A 102:18730–18735
Kumar V, Pandita S, Sidhu GPS, Sharma A, Khanna K, Kaur P, Bali AS, Setia R (2021) Copper bioavailability, uptake, toxicity and tolerance in plants: a comprehensive review. Chemosphere 262:127810
Kupper H, Götz B, Mijovilovich A, Küpper FC, Meyer-Klaucke WE (2009) Complexation and toxicity of copper in higher plants I. Characterization of copper accumulation, speciation, and toxicity in Crassula helmsii as a new copper accumulator. Plant Physiol 151:702–714
Lanquar V, Lelièvre F, Bolte S, Hamès C, Alcon C, Neumann D et al (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–4051. https://doi.org/10.1038/sj.emboj.7600864
Li JY, Liu J, Dong D, Jia X, McCouch SR, Kochian LV (2014) Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance. Proc Natl Acad Sci U S A 111:6503. https://doi.org/10.1073/pnas.1318975111
Lippard SJ, Berg JM (1994) Principles of bioinorganic chemistry. University Science Books, New York
Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London
Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H et al (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667. https://doi.org/10.1104/pp.126.4.1646
Mir AR, Pichtel J, Hayat S (2021) Copper: uptake, toxicity and tolerance in plants and management of Cu-contaminated soil. Biometals 34(4):737–759. https://doi.org/10.1007/s10534-021-00306-z
Monni S, Salemaa M, White C, Tuittila E (2000) Copper resistance of Calluna vulgaris originating from the pollution gradient of a Cu-Ni smelter, in southwest Finland. Environ Pollut 109:211–219
Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. Mol Cell Res 1763(7):609–620
Peña MMO, Lee J, Thiele DJ (1999) A delicate balance: homeostatic control of copper uptake and distribution. J Nutr 129:1251–1260
Perea-García A, Garcia-Molina A, Andrés-Colás N, Vera-Sirera F, Pérez-Amador MA, Puig S et al (2013) Arabidopsis copper transport protein COPT2 participates in the cross talk between iron deficiency responses and low-phosphate signaling. Plant Physiol 162:180–194
Printz B, Lutts S, Hausman JF, Sergeant K (2016) Copper trafficking in plants and its implication on cell wall dynamics. Front Plant Sci 7:601
Puig S (2014) Function and regulation of the plant COPT family of high-affinity copper transport proteins. Adv Bot 2014:476917
Puig S, Thiele DJ (2002) Molecular mechanisms of copper uptake and distribution. Curr Opin Chem Biol 6:171–180. https://doi.org/10.1016/S1367-5931(02)00298-3
Puig S, Andres-Colas N, Garcia-Molina A, Penarrubia L (2007a) Copper and iron homeostasis in Arabidopsis: response to metal deficiencies, interactions and biotechnological applications. Plant Cell Environ 30:271–290. https://doi.org/10.1111/j.1365-3040.2007.01642.x
Puig S, Mira H, Dorcey E et al (2007b) Higher plants possess two different types of ATX1-like copper chaperones. Biochem Biophys Res Commun 354:385–390
Qin L, Han P, Chen L, Walk TC, Li Y, Hu X, Xie L, Liao H, Liao X (2017) Genome-wide identification and expression analysis of NRAMP family genes in soybean (Glycine Max L.). Front Plant Sci 8:1436
Rehman N, Maqbool Z, Peng D, Liu L (2019) Morpho-physiological traits, antioxidant capacity and phytoextraction of copper by ramie (Boehmeria nivea L.) grown as fodder in copper-contaminated soil. Environ Sci Pollut Res 26:5851–5861
Salt DE, Smith RD, Raskin I, Annu. (1998) Phytoremediation. Annu Rev Plant Physiol 49:643–668
Sancenon V, Puig S, Mateu-Andres I, Dorcey E, Thiele DJ, Penarrubia L (2004) The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. J Biol Chem 279:15348–15355. https://doi.org/10.1074/jbc.M313321200
Sanz A, Pike S, Khan MA et al (2019) Copper uptake mechanism of Arabidopsis thaliana high-affinity COPT transporters. Protoplasma 256:161–170
Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 Is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167. https://doi.org/10.1105/tpc.112.096925
Shikanai T, Müller-Moulé P, Munekage Y et al (2003) PAA1, a P-Type ATPase of Arabidopsis, functions in copper transport in chloroplasts. Plant Cell 15:1333–1346
Shin LJ, Yeh KC (2012) Overexpression of Arabidopsis ATX1 retards plant growth under severe copper deficiency. Plant Signal Behav 7:1082–1083
Shin L-J, Lo J-C, Ye K-C (2012) Copper chaperone antioxidant protein1 is essential for copper homeostasis. Plant Physiol 159(3):1099–1110
Solioz M, Vulpe C (1996) CPx-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem Sci 21(7):237–241
Sommer F, Kropat J, Malasarn D, Grossoehme NE, Chen X, Giedroc DP et al (2010) The CRR1 nutritional copper sensor in Chlamydomonas contains two distinct metal-responsive domains. Plant Cell 22:4098–4113
Takahashi R, Ishimaru Y, Nakanishi H, Nishizawa NK (2011) Role of the iron transporter OsNRAMP1 in cadmium uptake and accumulation in rice. Plant Signal Behav 6:1813–1816. https://doi.org/10.4161/psb.6.11.17587
Tejada-Jiménez M, Castro-Rodríguez R, Kryvoruchko I, Lucas MM, Udvardi M, Imperial J et al (2015) Medicago truncatula natural resistance-associated macrophage protein1 is required for iron uptake by rhizobia-infected nodule cells. Plant Physiol 168:258–272. https://doi.org/10.1104/pp.114.254672
Waters BM, Chu HH, Didonato RJ, Roberts LA, Eisley RB, Lahner B, Salt DE, Walker EL (2006) Mutations in Arabidopsis yellow stripe-like 1 and yellow stripe-like 3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141:1446–1458. https://doi.org/10.1104/pp.106.082586
Williams LE, Mills RF (2005) P1B-ATPases-an ancient family of transition metal pumps with diverse function in plants. Trends Plant Sci 10:491–502. https://doi.org/10.1016/j.tplants.2005.08.008
Williams LE, Pittman JK, Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. Biochim Biophys Acta 1465:104–126. https://doi.org/10.1016/S0005-2736(00)00133-4
Wintz H, Fox T, Wu Y-Y, Feng V, Chen W, Chang H-S et al (2003) Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J Biol Chem 278:47644–47653
Woeste KE, Kieber JJ (2000) A strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype. Plant Cell 12:443–455
Xiong H, Kobayashi T, Kakei Y, Senoura T, Nakazono M, Takahashi H et al (2012) AhNRAMP1 iron transporter is involved in iron acquisition in peanut. J Exp Bot 63:4437–4446. https://doi.org/10.1093/jxb/ers117
Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T et al (2004) A novel zinc-binding motif revealed by solution structures of DNA-binding domains of Arabidopsis SBP-family transcription factors. J Mol Biol 337:49–63
Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Biol Chem 282:16369–16378
Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361
Yang M, Zhang W, Dong H, Zhang Y, Lv K, Wang D et al (2014) OsNRAMP3 is a vascular bundles-specific manganese transporter that is responsible for manganese distribution in rice. PLoS ONE 8:e83990. https://doi.org/10.1371/journal.pone.0083990
Yruela I (2005) Copper in plants. Braz J Plant Physiol 17:145–156
Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36(5):409–430
Yuan M, Chu Z, Li X, Xu C, Wang S (2010) The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution. Plant Cell 22:3164–3176. https://doi.org/10.1105/tpc.110.078022
Yuan M, Li X, Xiao J, Wang S (2011) Molecular and functional analyses of COPT/Ctr-type copper transporter-like gene family in rice. BMC Plant Biol 11(1):1–12
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Gul, A., Haq, N., Rafique, K. (2022). The Copper Transport Mechanism in Plants. In: Kumar, K., Srivastava, S. (eds) Plant Metal and Metalloid Transporters. Springer, Singapore. https://doi.org/10.1007/978-981-19-6103-8_13
Download citation
DOI: https://doi.org/10.1007/978-981-19-6103-8_13
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-19-6102-1
Online ISBN: 978-981-19-6103-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)