TRENDS in Plant Science Vol.7 No.4 April 2002 http://plants.trends.com 1360-1385/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S1360-1385(02)02241-0 162 Review Günter Neumann* Institut für Planzenernährung (330), Universität Hohenheim, 70593 Stuttgart, Germany. *e-mail: gd.neumann@ t-online.de Enrico Martinoia Laboratoire de Physiologie Végétale, Institut de Botanique, Université de Neuchâtel, Rue Emile Argand 13, CH-2007 Neuchâtel, Switzerland. Cluster roots [1] are bottlebrush-like clusters of rootlets with limited growth that arise from the pericycle opposite the protoxylem poles along the lateral roots in many species of the Proteaceae [2]. In many cases, members of this family are slow- growing sclerophyllous shrubs and trees, and a major component of the Mediterranean flora in Western Australia and South Africa. They are adapted to habitats of extremely low soil fertility, such as highly leached sands, sandstones and laterites, with phosphorus (P) as a major limiting nutrient for plant growth [3]. Cluster roots have been functionally linked with an efficient chemical mobilization of sparingly soluble soil P sources by organic chelators (e.g. citrate, malate and phenolics) and ectoenzymes (acid phosphatase) released into the rhizosphere of root clusters in extraordinarily high quantities (Figs 1 and 2) [4–7]. Slow growth rates and an efficient internal P use, with seasonal separation of P uptake and storage mainly during the winter rain period and P use for shoot growth during spring and summer [8], are considered to be additional important determinants for P efficiency in members of the Proteaceae. Apart from the 236 species in 27 genera of the Proteaceae, cluster roots are also formed in some members of the Betulaceae, Casuarinaceae, Cucurbitaceae, Cyperaceae, Eleagnaceae, Leguminosae, Moraceae, Myricaceae and Restionaceae, which are all adapted to low fertility soils [2]. Cluster-rooted plant species frequently exhibit N 2 fixation via Rhizobia and Frankia symbiosis but, in most cases, mycorrhizal associations are lacking. Chemical mobilization of nutrients by root exudates released in huge amounts from individual root clusters over a limited time period of 1–3 days (Fig. 3) [4,9,10] might be an alternative strategy to nutrient acquisition via mycorrhizal associations. The rapid development of cluster roots within several days could be an advantage, particularly in seasonally arid climates where the establishment of functionally active mycorrhizae, which usually requires longer periods of time, might be biased by limited periods of rainfall. Therefore, along with mycorrhizae and N 2 -fixing nodules, cluster roots are postulated to be the third major adaptation for nutrient acquisition in terrestrial vascular sporophytes [2]. Induction and development of cluster roots Formation of cluster roots appears to be mainly induced by a shortage of P and, at least in some plant species, by Fe deficiency [3,11–13]. Experiments with foliar and split-root P application have shown that cluster root formation is at least partially triggered by a low internal P status of the plant [14,15]. However, in many cases, a high and sometimes even phytotoxic P supply is necessary for complete depression of cluster root development [3,6]. Nevertheless, cluster root formation seems to be stimulated in nutrient-rich patches [1,16] and in upper soil layers rich in organic matter [17], suggesting that external factors are also involved. This has been attributed to the proliferation of lateral roots as a response to localized nutrient supply, which are the sites of cluster root initiation [16]. Additionally, certain constituents of dissolved organic matter, the pH of the growth medium, as well as microbial factors, might exert some stimulatory effects but are probably not obligatory for the development of cluster roots [3,18,19]. Also, differences in the pattern of cluster root formation between plant species cannot be excluded. In addition, auxin–cytokinin interactions have been implicated in cluster root formation, with auxin application having a promoting effect and auxin antagonists and cytokinins having an inhibitory effect [10,20,21]. Accordingly, characterization of cluster root expressed sequence tags (ESTs) associated with plant hormones revealed down-regulation of an EST with homology to indole acetic acid (IAA) glycosyltransferase and up-regulation of a zeatin glycosyltransferase [22], both enzymes involved in the inactivation of auxins (e.g. IAA) and cytokinins (e.g. zeatin), respectively. Moreover, enhanced expression of an EST with Cluster roots are a characteristic of members of the Proteaceae and of several other plant species that are adapted to habitats of extremely low soil fertility, usually without formation of mycorrhizal associations. Functionally linked w ith intense mobilization of nutrients (P , Fe, Zn, Mn) by root-induced chemical changes (pH, root exudates, redox potential) in the rhizosphere, cluster-rooted plant species can serve as model plants to study rhizosphere processes and regulatory aspects of plant adaptations for chemical mobilization of nutrients in the rhizosphere. Published online: 14 March 2002 Cluster roots – an underground adaptation for survival in extreme environments Günter Neumann and Enrico M artinoia