R E V I E W S Q The role of iron in plant host-pathogen interactions Dominique Expert, Corine Enard and Celine Masclaux I ron is essential for virtually all forms of life. Owing to the ability of atomic iron to generate two stable ionic species, ferric iron (Fe3+) and ferrous iron (Fe2+), iron acts as a catalyst in numerous biologi- cal redox reactions of funda- mental importance. However, iron can catalyse the formation of extremely reactive free radi- cals in the presence of oxygen, and can trigger chain reactions that are harmful to biomol- ecules 1,2. Its high reactivity means that iron is never present Iron is unlikely to be readily available in plant tissues for invading microorganisms. Soft rot, caused by Erwinia chrysanthemi strain 3937 on African violets, is a valuable model for studying the role of iron and its ligands in plant-pathogen interactions. These studies could lead to the development of new control strategies against microbial infections of plants. D. Expert*, C. Enard and C. Masclaux are in the Laboratoire de Pathologie vdgStale, INRA/INA P-G, 16 rue Claude Bernard, 75231 Paris Cedex 05, France. *tek +33 1 44 08 17 06, fax: +33 1 44 08 1631, e-mail: expert@inapv.inapg.inra.fr in biological tissues as a free element; it is not there- fore readily accessible to intruding microorganisms. Ferritins store iron in a nontoxic form surrounded by a protein shell. Animal and plant ferritins can contain up to 4500 Fe 3*ions coprecipitated with phosphate in a ferrihydrate form 3. Bacterioferritins contain haem; their role in protecting bacteria from iron overload is questionable 4. How is iron mobilized within the plant? In water- conducting xylem vessels, Fe 3÷is bound to organic acids, mainly in the form of citrate and malate s. In the food-conducting phloem vessels, an Fe2+chelate of the amino acid nicotianamine has been found 6. Nicotian- amine is a ubiquitous plant constituent; a nicotian- amine-free tomato mutant has been found to show typi- cal symptoms of iron deficiency, with chlorosis visible between the veins on leaves 7. Although no clear func- tion has yet been demonstrated for nicotianamine, this ligand is thought to transport Fe z+ ions over short distances within the plant. Long-distance transport in the xylem is thought to involve iron bound to a pep- tide or some other organic substrate 8. The status of iron in the extracellular space (apoplast) is still unknown. Higher plants, except grasses, acquire iron from the soil by inducing a complex physiological response 9 involving a plasma-membrane-bound ferric chelate re- ductase at the root surface. An efflux of protons and phenolic reductants makes iron more soluble in the vicinity of the root. In contrast, grasses secrete sidero- phores 1°, such as mugineic acid. Mugineic acid has an affinity for Fe3+(K~,the formation constant of the ferri- siderophore) of 10 TM (compared with a Kf of 103°-1050 for common microbial siderophores). The iron-transporting transferrins in vertebrate body fluids act not only as specific Fe3+ transporters, but also as powerful iron scavengers 11.The discovery more than 40years ago of the bacterio- static effect of egg white, result- ing from iron chelation by ovo- transferrin, was the starting point for numerous studies of the role of iron in infectious diseases 12. Many host defences aim to withhold nutritional iron from animal pathogens, while microorganisms have evolved specific iron-transport mecha- nisms to extract iron from the host 13'14. Although some micro- organisms have evolved highly specialized routes to acquire iron (such as outer-membrane transferrin receptors), the production of siderophores as high-affinity Fe3+-scavenging compounds remains a common strategy in animal pathogens. The produc- tion of siderophores greatly benefits the pathogen be- cause these molecules can remove iron from a variety of mineral and organic substrates. All plants lack transferrin or transferrin-like proteins. The vascular and apoplastic fluids are a hostile environment for plant pathogens. Iron is a limiting growth factor for microorganisms because micro- molar concentrations of iron are necessary to support multiplication. At physiological pH, there is insuffi- cient free iron available for microorganisms because of the extremely low solubility of Fe-3+ (10-18M). A wide- spread strategy in plant pathogens to increase the iron availability is to produce siderophores. The role of iron in pathogenicity has been investigated genetically and the siderophore structurally characterized in a few cases. Nevertheless, siderophores have not yet been implicated in the pathogenesis of plant disease, except in the cases of Erwinia chrysanthemi is and Erwinia amylovora (D. Expert, A. Dellagi and J-P. Paulin, unpublished). As in animal infections, the role of siderophores in the virulence of plant pathogens seems to be more subtle than might be expected, and is intimately related to the life cycle of the pathogen within its host. The avail- ability of iron limits substantial growth and movement of bacteria inside the plant. In this article, we describe studies that illustrate how iron limits the activities of plant pathogens, with special emphasis on the disease caused by E. chrysanthemi, for which the control of iron homeostasis is known to be central to pathogenicity. iron in the pathogenosis of plant pathogens Smut disease is an interesting pathology of maize caused by Ustilago maydis. This basidiomycete fungus induces Copyright C) 1996 Elsevicr Science Ltd, All rights reserved. 0966 842X/96/$15.00 HIz S0966-842X(96)10038-X TRENDS IN MI(]R()BIC)LOGY 232 voL. 4 No. 6 JUNE 1 996