A Comparative Inventory of Metal Transporters in the Green Alga Chlamydomonas reinhardtii and the Red Alga Cyanidioschizon merolae    

Abstract

As in all organisms, metal cations are crucial for nutrition in plants. Several metals, such as copper, iron, zinc, and manganese, act as important cofactors for many enzymes and are essential for both mitochondrial and chloroplast functions. However, when supplied in excess, these essential cations can become toxic, like heavy metals with no generally established function, such as cadmium, lead, or mercury. To maintain micronutrient metal homeostasis and to cope with the deleterious effects of nonessential heavy metals, plants have developed a complex network of metal uptake, chelation, trafficking, and storage processes. Metal transporters are required to maintain metal homeostasis and thus constitute important components of this network (Clemens, 2001;Hall and Williams, 2003).In recent years, a number of membrane transport protein families have been implicated in metal homeostasis in plants. These include the cation diffusion facilitators (CDF), the Zrt-, Irt-like proteins (ZIP), the cation exchangers (CAX), the copper transporters (COPT), the heavy-metal P-type ATPases (HMA), the natural resistance-associated macrophage proteins (NRAMP), and the ATP-binding cassette (ABC) transporters (Williams et al., 2000;Maser et al., 2001;Cobbett et al., 2003;Hall and Williams, 2003). These transporters are encoded by multigene families. For example, 15 ZIP genes, 12 metal tolerance protein (MTP) genes, and 8 HMA genes are present in the Arabidopsis (Arabidopsis thaliana) genome (Cobbett et al., 2003;Delhaize et al., 2003). However, the transport specificities, patterns of expression, or subcellular localizations of metal transport proteins are still largely unknown. To further understand plant metal homeostasis, it will be necessary to elucidate the contribution of each of these transporters to the uptake, trafficking, and storage of essential metals, as well as to the detoxification of toxic heavy metals.In this article, we present an overview of our current knowledge of the metal transport function in metal homeostasis and tolerance in eukaryotes, with a special emphasis on plants. We also provide a timely inventory of putative metal transporters in two unicellular algal models, the green alga Chlamydomonas reinhardtii and the red alga Cyanidioschizon merolae. These new data should facilitate functional genomics and molecular analysis of metal homeostasis and tolerance in photosynthetic organisms. Moreover, the comparison of metal transporters from species belonging to the red and green algae with those of the land plant Arabidopsis, as well as with their human and yeast homologs, allows some light to be shed on the molecular evolution of metal homeostasis and tolerance systems. TWO UNICELLULAR ALGAL MODEL SYSTEMS

Transition metal transport

“…Group III CDF proteins are most likely Zn transporters [21]. MTP1 has been identified in transcriptomic approaches as a candidate gene in shoots and roots of A. halleri and in roots of T. caerulescens.…”

“…Their comparison reveals that unicellular algae possess the basic tools to maintain cellular metal homeostasis. As such, they represent powerful models to study the functions and the interactions of different metal transport and intracellular trafficking systems [21]. However, higher plants evolved adaptations of their metal homeostasis network reflecting the need for long-distance transport and for the proper distribution of metals between different organs and cell types.…”

“…A discontiguous MegaBLAST search did not retrieve sequences homologous to the divalent cation-transporting P 1B -type ATPases in the moss Physcomitrella patens in the NCBI trace archives (January 2007). Similarly, unicellular algae only possess the Cu(I)-transporting P IB -type ATPases that are involved in copper delivery to the chloroplast or the ER, but lack the divalent cation-transporting HMAs [17,21].…”

“…Recently, AtIREG2 was shown to have a role in nickel transport into the vacuole under irondeficiency [68]. An IREG1 homolog is also present in the genome of the unicellular red alga Cyanidioschyzon merolae, but is lacking in Chlamydomonas reinhardtii and S. cerevisiae [21].…”

“…Finally, putative transporters of metal ion ligands, the AtFRD3 (Ferric Reductase Defective 3) of the large multidrug and toxin efflux (MATE) family and AtZIF1 (Zinc Induced Facilitator 1) of the major facilitator superfamily (MFS), have key roles in iron and Zn homeostasis, respectively [11][12][13]. These plant metal transporter families and their biological roles have been reviewed by other authors recently [2,[14][15][16][17][18][19][20][21] (review Iron Transport, this issue).…”