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Induction of Jasmonate Biosynthesis in ... - Plant Physiology

Induction of Jasmonate Biosynthesis in ... - Plant Physiology

Induction of Jasmonate Biosynthesis in ... - Plant

Induction of Jasmonate Biosynthesis in Arbuscular Mycorrhizal Barley Roots 1,2 Bettina Hause*, Walter Maier, Otto Miersch, Robert Kramell, and Dieter Strack Abteilung Sekundärstoffwechsel (B.H., W.M., D.S.) and Abteilung Naturstoff-Biotechnologie (O.M., R.K.), Leibniz-Institut für Pflanzenbiochemie, D–06120 Halle (Saale), Germany Colonization of barley (Hordeum vulgare cv Salome) roots by an arbuscular mycorrhizal fungus, Glomus intraradices Schenck & Smith, leads to elevated levels of endogenous jasmonic acid (JA) and its amino acid conjugate JA-isoleucine, whereas the level of the JA precursor, oxophytodienoic acid, remains constant. The rise in jasmonates is accompanied by the expression of genes coding for an enzyme of JA biosynthesis (allene oxide synthase) and of a jasmonate-induced protein (JIP23). In situ hybridization and immunocytochemical analysis revealed that expression of these genes occurred cell specifically within arbuscule-containing root cortex cells. The concomitant gene expression indicates that jasmonates are generated and act within arbuscule-containing cells. By use of a near-synchronous mycorrhization, analysis of temporal expression patterns showed the occurrence of transcript accumulation 4 to 6 d after the appearance of the first arbuscules. This suggests that the endogenous rise in jasmonates might be related to the fully established symbiosis rather than to the recognition of interacting partners or to the onset of interaction. Because the plant supplies the fungus with carbohydrates, a model is proposed in which the induction of JA biosynthesis in colonized roots is linked to the stronger sink function of mycorrhizal roots compared with nonmycorrhizal roots. Arbuscular mycorrhizas (AMs) are the most common type of mycorrhizas (for review, see Smith and Read, 1997). AMs are formed between roots of more than 80% of all terrestrial plant species and Zygomycete fungi from the order Glomales. The fungus is able to grow into the root cortex by forming intraradical hyphae, which are subsequently differentiated into highly branched structures, the arbuscules, within cortex cells. Intraradical hyphae and arbuscules are responsible for exchange of nutrients between the plant and the fungus. The plant supplies the fungus with carbohydrates, whereas the fungus assists the plant with the acquisition of phosphate and other mineral nutrients from the soil (Harrison, 1998). The beneficial effects of the AM symbiosis result from a complex molecular dialogue between the two symbiotic partners (Harrison, 1999). Some processes occurring in this dialogue are known to be mediated by phytohormones on the plant side. However, most of these phytohormone effects were suggested from application experiments (Barker and Tagu, 2000). A possible role for abscisic acid in the establishment of mycorrhiza was suggested from the fact that the endogenous content of abscisic acid was increased in mycorrhizal roots, but not in non- 1 This work was supported by the Deutsche Forschungsgemeinschaft (grant no. HA2655/4–1 in SPP1084) and by Fonds der Chemischen Industrie. 2 This paper is dedicated to Prof. Dr. Benno Parthier on the occasion of his 70th birthday. * Corresponding author; e-mail bhause@ipb-halle.de; fax 49– 345–55821219. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.006007. mycorrhizal roots (Bothe et al., 1994). In a previous study, the establishment of AM in barley (Hordeum vulgare) roots was shown to be accompanied by the accumulation of putrescine and agmatine amides of 4-coumarate and ferulate, respectively, compounds that are also accumulated upon treatment of nonmycorrhizal barley roots with jasmonates (Peipp et al., 1997). This suggests a possible role of jasmonates in AM formation. Jasmonic acid (JA) and its derivatives, commonly termed jasmonates, are hormonal regulators involved in plant responses to abiotic and biotic stresses, as well as in plant development (Creelman and Mullet, 1997; Wasternack and Parthier, 1997). The role of jasmonates is well established as part of a complex signal transduction pathway activated upon local wounding of leaves (Ryan, 2000). Levels of endogenous jasmonate increase upon wounding and are followed by activation of genes involved in plant defense responses such as those coding for proteinase inhibitors, enzymes of phytoalexin synthesis, vegetative storage proteins, thionins, and defensins (Creelman and Mullet, 1997; Farmer et al., 1998; Ryan, 2000). However, it is less well understood how the rise of jasmonates is regulated. The elevation of jasmonate levels is usually correlated with the activation of genes coding for JA biosynthetic enzymes (for review, see Wasternack and Hause, 2002). The biosynthesis of JA (Fig. 1) starts with the insertion of oxygen at position 13 of �-linolenic acid catalyzed by 13-LOX. The resulting hydroperoxide is converted by AOS into an unstable allene oxide that can rapidly be degraded in vitro by chemical hydrolysis. Under cellular conditions, the allene oxide is Plant Physiology, November 2002, Vol. 130, pp. 1213–1220, www.plantphysiol.org © 2002 American Society of Plant Biologists 1213

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