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WHOLE PLANT AND ECOPHYSIOLOGY

Developmental Physiology of Cluster-Root Carboxylate Synthesis and Exudation in Harsh Hakea. Expression of Phosphoenolpyruvate Carboxylase and the Alternative Oxidase¹

School of Plant Biology, Faculty of Natural and Agricultural Sciences (M.W.S., M.D.C., S.F.-N., G.R.C., H.L.); and School of Biomedical and Chemical Sciences, Faculty of Life and Physical Sciences (H.M., D.A.D.), The University of Western Australia, Crawley, Western Australia 6009, Australia

Harsh hakea (Hakea prostrata R.Br.) is a member of the Proteaceae family, which is highly represented on the extremely nutrient-impoverished soils in southwest Australia. When phosphorus is limiting, harsh hakea develops proteoid or cluster roots that release carboxylates that mobilize sparingly soluble phosphate in the rhizosphere. To investigate the physiology underlying the synthesis and exudation of carboxylates from cluster roots in Proteaceae, we measured O₂ consumption, CO₂ release, internal carboxylate concentrations and carboxylate exudation, and the abundance of the enzymes phosphoenolpyruvate carboxylase and alternative oxidase (AOX) over a 3-week time course of cluster-root development. Peak rates of citrate and malate exudation were observed from 12- to 13-d-old cluster roots, preceded by a reduction in cluster-root total protein levels and a reduced rate of O₂ consumption. In harsh hakea, phosphoenolpyruvate carboxylase expression was relatively constant in cluster roots, regardless of developmental stage. During cluster-root maturation, however, the expression of AOX protein increased prior to the time when citrate and malate exudation peaked. This increase in AOX protein levels is presumably needed to allow a greater flow of electrons through the mitochondrial electron transport chain in the absence of rapid ATP turnover. Citrate and isocitrate synthesis and accumulation contributed in a major way to the subsequent burst of citrate and malate exudation. Phosphorus accumulated by harsh hakea cluster roots was remobilized during senescence as part of their efficient P cycling strategy for growth on nutrient impoverished soils.

² Permanent address: Department of Botany, University of Cape Town, Private Bag, Rondebosch 7701, South Africa.

³ Present address: Department of Biology, Graduate School of Science, Osaka University, 1–16 Machikaneyama, Toyonaka, Osaka 560–0043, Japan.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.035659.

^* Corresponding author; e-mail mshane{at}agric.uwa.edu.au; fax 61–8–6488–1108.

Received November 2, 2003; returned for revision February 16, 2004; accepted February 22, 2004.

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