Biol Cell (1995) 84,69-X1 0 Elsevier, Paris 69 Original article Cellular and molecular aspects of iron metabolism in plants Jean-Fraqois Briat, Isabelle Fobis-Loisy, Nicole Grignon, StCphane LobrCaux, Nadine Pascal, Gil Savino, SCverine Thoiron, Nicolaus von WirCn, Olivier Van Wuytswinkel Laboratoire de Biochimie et Physiologie Vkgktales, Centre National de la Recherche Scientifque (Unite’ de Recherche 573), Institut National de la Recherche Agronomique et ikole Nationale Supe’rieure d’Agronomie, Place Viala, F-34060 Montpellier Cedex I, France (Received 5 April 1995; accepted 2 June 1995) Summary - Iron is an essential element for plant metabolism because of its redox properties. Its long distance and intracellular traf- ficking requirespecialized proteins andlow molecular mass chelates because of its insolubility andtoxicity in presence of oxygen. Iron deficiency induces variousmorphological and biochemical changes. They includeroot hair morphogenesis, differentiation of rhizoder- ma1 cells into transfer cells, yellowing of leaves and ultrastructural disorganisation of chloroplasts and mitochondria, as well as increased synthesis of organic acidsand phenolics, and activation of root systems responsible for an enhanced iron uptakecapacity. Upon iron resupply, these alterations disappeared within few days and a transient accumulation of the iron storage protein ferritin in the plastids is one of the early events in this process. Iron excess can alsooccur in plantswhereit elicits an oxidative stress leading to necrotic spots in the leaves. Induction of ferritin synthesis is againan early eventof the plant response to this iron toxicity. Plant hor- mones suchas auxin, abscisic acid and ethylene, aswell asreactive oxygen intermediates play an importantrole in the transduction pathways, allowing plants to respond to these iron-deficiency and excess stresses. Similarities and differencesamong the various mechanisms responsible for iron uptakeandstorage in mammals, higherplantsandyeastare outlined. Relationships between iron and copper metabolism arealso indicated. plant / root / chloroplast / iron / ferritin Introduction Metal ion homeostasis is strictly controlled in both prokar- yotic and eukaryotic cells for essential and non-essential mineral nutrients. In order to maintain cellular ion homeo- stasis when the extracellular concentration of metal ions varies, a series of regulatory mechanisms has evolved. They involve a coordinate control of the synthesis of transport, binding and storage proteins in response to a given metal ion concentration in the environment. Metal ion concentra- tions are also spatially and temporary regulated in pluricel- lular organisms. Using various model systems, important progress has been made in recent years towards the under- standing of the mechanisms controlling the expression of genes which are involved in metal ion homeostasis, and the role that metal ions play themselves in these regulatory pathways [49,gO, 1271. In plants, mineral nutrition is one of the factors involved in growth and development and, therefore, in crop produc- tivity. Among essential mineral elements, iron plays an important role because of its implication in fundamental processes such as photosynthesis, respiration, nitrogen fixa- tion and DNA synthesis. In addition, it acts as a cofactor of key enzymes involved in plant hormone synthesis (lipoxy- genases and ethylene forming enzymes for example) [9, 1111 which are involved in various pathways controlling both developmental events and responses to multiple envi- ronmental variations. The importance of iron in the various biological mechanisms mentioned above can be explained by the fact that this element, at physiological pH in aqueous phase, can exist under two redox states (ferrous, Fe*+, or ferric, Fe3+) allowing its participation in numerous reactions involving electron transfers. In presence of oxygen, how- ever, iron insolubility and toxicity, through free radical pro- duction by reactivity with reduced oxygen intermediates, are major problems for the use of this element by living organisms [126]. Therefore, iron traffic in plants has to be strictly controlled, and various molecules chelating iron are involved in these mechanisms. In addition, plants have to face great differences in iron availability in the environment because of their immobility, and either starvation or excess of this element can be responsible for severe nutritional dis- orders affecting deeply the physiology of plants [36,91]. In order to respond to these stresses, plant cells produce sig- nals, most of them being still uncharacterized, which partic- ipate to the activation of specific genetic programs involved: i) in the control of iron uptake by roots; ii) in long distance iron transport between roots and shoots; iii) in sensing the iron status in the leaves and signalling it to the roots; iv) in iron subcellular distribution; and v) in detoxifying and buffering iron in case of excess (fig 1). The principal aim of this review is to summarize our actual knowledge on the cellular and molecular processes in iron metabolism of plants grown with adequate supply of iron or under iron stress (deficiency or excess). Iron traffk in non-stressedplants The mechanism of Fe uptake by plant roots depends highly on the redox state and binding form of iron. Under reducing environmental conditions (for example, reduced microsites or paddy soils), iron predominantly occurs as ferrous iron and can be directly taken up by the roots, presumably via a