Copper Trafficking in Plants and Its Implication on Cell Wall Dynamics

Abstract

In plants, copper (Cu) acts as essential cofactor of numerous proteins. While the definitive number of these so-called cuproproteins is unknown, they perform central functions in plant cells. As micronutrient, a minimal amount of Cu is needed to ensure cellular functions. However, Cu excess may exert in contrast detrimental effects on plant primary production and even survival. Therefore it is essential for a plant to have a strictly controlled Cu homeostasis, an equilibrium that is both tissue and developmentally influenced. In the current review an overview is presented on the different stages of Cu transport from the soil into the plant and throughout the different plant tissues. Special emphasis is on the Cu-dependent responses mediated by the SPL7 transcription factor, and the crosstalk between this transcriptional regulation and microRNA-mediated suppression of translation of seemingly non-essential cuproproteins. Since Cu is an essential player in electron transport, we also review the recent insights into the molecular mechanisms controlling chloroplastic and mitochondrial Cu transport and homeostasis. We finally highlight the involvement of numerous Cu-proteins and Cu-dependent activities in the properties of one of the major Cu-accumulation sites in plants: the cell wall.

Keywords: cell wall; copper; plant; transport.

FIGURE 1

SPL7-regulation network and existing interactions in plants. HY5, BZip transcription factor ELONGATED HYPOCOTYL 5; KIN17, Kin17 DNA and RNA Binding Protein; NLS, nuclear localization signal; SBP-domain, SQUAMOSA promoter binding proteins-domain; SOD, superoxide dismutase; SPL7, SQUAMOSA promoter-binding protein-like 7 transcription factor; TMD, transmembrane domain.

FIGURE 2

Overview of the Cu-transport system occurring at the root tip of dicots. Copper is taken up in the roots in its reduced form Cu⁺ by COPT proteins, highly selective Cu-transporters. Alternative, but still controversial, Cu uptake system may be non-selective ZIP proteins whereas Cu²⁺-efflux is mediated by H⁺/Cu²⁺ antiporters. In the cytosol, free Cu⁺ induces the generation of ROS thereby opening NSCCs, allowing the entry of Ca²⁺ and inducing root growth. Cu may further modulate root growth through interaction with auxin efflux carrier PIN1 and with the multi-copperoxidases LPR1/2. In case excessive Cu enters the roots, the massive generation of ROS activates also the efflux of K⁺ through NSCC, causing activation of Programmed Cell Death (PCD). ROS can be quenched by the acitivty of CSD1 which acquires Cu from CCS. To prevent ROS generarion, Cu⁺ is usually chelated by intracellular MTs or specific chaperones ATX1. Cu-transport to extracellular compartments in mediated by HMA5 proteins. In the phloem and in the xylem, Cu in transported in Cu(II)-complexes or Cu(I)-MT complexes. ATX1, antioxidant protein 1; COPT1/2, Cu transporter 1/2; CCS, Cu-chaperones to Cu/Zn superoxide dismutase; CSD1, cytosolic Cu/Zn superoxide dismutase; FRO 4/5, ferric reductase oxidase 4/5; LPR1/2, low phosphate response multi-copperoxidase 1/2; MT, metallothioneins; NSCC, non-selective cationic channels; OsHMA5/AtHMA5, Oryza sativa heavy metal ATPase 5/Arabidopsis thaliana heavy metal ATPase 5; PCD, programmed cell death; PIN1, pin-formed 1; ROS, reactive oxygen species; ZIP, Zrt- and Irt-like protein.

FIGURE 3

A model of the long-distance system for Cu-transport. Copper ions are transported in the vasculature in the form of Cu(I)-MT or Cu(II)-complexes. Prior to leaf cellular uptake, Cu²⁺ is reduced to Cu⁺ by FRO4 and enters the leaf cell by COPT6 proteins. Cu remobilization from senescing tissues is performed via YSL proteins. In particular YSL proteins similar to YSL16 in O. sativa are involved in the transport of Cu from Cu(II)-complexes from senescing organs to the phloem. A possible involvement of CCH in Cu remobilization from old to young tissues has also been envisaged. Remobilized-Cu is transferred to sink organs via YSL-proteins such as YSL2 for the transport of Cu(II)-complexes and probably YSL1/3 for Cu(I)-MT transport. CCH, Cu chaperone; COPT6, Cu transporter 6; FRO4, ferric reductase oxidase 4; MT, metallothioneins; YSL, Yellow Stripe Like.

FIGURE 4

Overview of some cell-wall loosening/strengthening mechanisms relying on the presence of Cu.