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Brassinosteroid and Systemin: Two Hormones Perceived by the Same Receptor

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Brassinosteroid and Systemin: Two Hormones Perceived by the Same Receptor 102 Update TRENDS in Plant Science Vol.8 No.3 March 2003 10 Voesenek, L.A.C.J. et al. (1999) A lack of aerenchyma and high regions which confer muscle-specific gene expression. J. Mol. Biol. 278, rates of radial oxygen loss from the root base contribute to the 167–181 waterlogging intolerance of Brassica napus. Aust. J. Plant Physiol. 26, 19 Kauffman, S.A. (1969) Homeostasis and differentiation in random 87–93 genetic control networks. Nature 224, 177–178 11 Dolferus, R. et al. (1994) Differential interactions of promoter elements 20 De Jong, H. (2002) Modeling and simulation of genetic regulatory in stress responses of the Arabidopsis Adh gene. Plant Physiol. 105, systems: a literature review. J. Comput. Biol. 9, 67–103 1075–1087 21 Lee, T.I. et al. (2002) Transcriptional regulatory networks in 12 Harmer, S.L. et al. (2000) Orchestrated transcription of key pathways Saccharomyces cerevisiae. 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(2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14, 1605–1619 15 Thijs, G. et al. (2002) A Gibbs sampling method to detect over- 26 Kauffman, S.A. (1993) Origins of Order–Self-Organization and represented motifs in upstream regions of coexpressed genes. Selection in Evolution, Oxford University Press J. Comput. Biol. 9, 447–464 27 Lieb, J.D. et al. (2001) Promoter-specific binding of Rap1 revealed by 16 Spellman, P.T. et al. (1998) Comprehensive identification of cell cycle- genome-wide maps of protein-DNA association. Nat. Genet. 28,327–334 regulated genes of the yeast Saccharomyces cerevisiae by microarray 28 Iyer, V.R. et al. (2001) Genomic binding sites of the yeast cell-cycle hybridization. Mol. Biol. Cell 9, 3273–3297 transcription factors SBF and MBF. Nature 409, 533–538 17 Bussemaker, H.J. et al. (2001) Regulatory element detection using correlation with expression. Nat. Genet. 27, 167–171 1360-1385/03/$ - see front matter q 2003 Elsevier Science Ltd. All rights reserved. 18 Wasserman, W.W. and Fickett, J.W. (1998) Identification of regulatory doi:10.1016/S1360-1385(03)00006-2 Brassinosteroid and systemin: two hormones perceived by the same receptor Miklos Szekeres Institute of Plant Biology, Biological Research Centre of the Hungarian Academy of Sciences, POB 521, H-6701 Szeged, Hungary Brassinosteroids, coordinating developmental events, nucleus, where they act as positive regulators of and systemin, inducing systemic wound responses to BR-responsive gene expression [2–4]. attacks by insect pests, are newly recognized plant Considerable attention has been focused on the func- hormones that are perceived by plasma membrane- tional characterization of BRI1, the putative BR receptor. localized leucine-rich repeat receptor kinases. The A series of elegant experiments revealed that the extra- recent characterization of the brassinosteroid receptor cellular portion of the protein is required for BR-dependent BRI1 from tomato revealed that this protein is identical activation of the intracellular, Ser/Thr-specific kinase to the previously isolated SR160 systemin receptor, domain [5,6]. Using radiolabelled BL, it was shown that strongly suggesting that both brassinosteroid and BRI1 co-immunoprecipitated with BL binding activity, but systemin signalling use the same surface receptor. hormone binding was prevented by mutations affecting the extracellular domain of the protein [7]. These data Brassinosteroids (BRs) are polyhydroxy-steroid phyto- unequivocally demonstrated that BRI1 is an essential hormones controlling important developmental functions, component of the BR receptor complex. such as growth, photomorphogenesis, fertility, seed ger- Recent cloning and sequence analysis of the tomato mination, senescence and stress tolerance [1].Brassinolide BRI1 gene (tBRI1) by Teresa Montoya and colleagues led (BL), the most active BR, was identified in 1979; several key to the exciting discovery that it encodes the Lycopersicon elements of its signalling pathway have now been charac- esculentum equivalent of the Lycopersicon peruvianum terized with the help of BR-response mutants. Perception of SR160 LRR receptor kinase [8], which had been identified BL by BRASSINOSTEROID INSENSITIVE 1 (BRI1), a as the receptor of the peptide hormone systemin [9]. plasma membrane-localized leucine-rich repeat (LRR) recep- tor kinase, probably initiates a phosphorylation cascade that Abs1 and Cu3 encode the tomato ortholog of BRI1 deactivates the cytoplasmic GSK3/SHAGGY-like BIN2 The BR-insensitive mutants of tomato, altered brassino- lide sensitivity 1 (abs1, from L. esculentum) [8] and curl 3 kinase, a negative regulator of BR signalling. By phosphor- (cu3, from Lycopersicon pimpinellifolium) [10] have simi- ylating BES1 and BZR1, two downstream components of lar phenotypic features, but abs1 is less dwarfed, develops the pathway, BIN2 can prevent their translocation to the an elongated root and retains its fertility and partial responsiveness to BL (Fig. 1). In both abs1 and cu3, Corresponding author: Miklos Szekeres ([email protected]). reverse-transcription PCR assays detected increased http://plants.trends.com Update TRENDS in Plant Science Vol.8 No.3 March 2003 103 N-terminal region 15 N-terminal LRRs 6 N-terminal LRRs flanking the island Island domain 4 C-terminal LRRs flanking the island Transmembrane region Kinase domain 0 25 50 75 100% TRENDS in Plant Science abs1 Wild type Fig. 2. Sequence conservation of structural regions between BRI1 proteins (with accession numbers) from Arabidopsis thaliana (AAC49810), rice (Oryza sativa; AP003453.3), tomato (Lycopersicon esculentum; AY179606) and pea (Pisum sati- –BL+BL –BL +BL vum) [8]. The blue bars corresponding to the indicated BRI1 regions show the per- centage of amino acid sequence identity, calculated as the average of the identity levels obtained by pair-wise alignments using the PileUp program. Abbreviation: LRR, leucine-rich repeat. Sequence conservation between BRI1 orthologs reveals structural requirements of BR perception BRI1 is a typical plasma membrane-localized receptor kinase with complex domain structure. The characteristic Fig. 1. Partial brassinosteroid-insensitive phenotype of the tomato (Lycopersicon extracellular (sensor) part with 25 LRR motifs, inter- esculentum) abs1 mutant. Three-week old abs1 and wild-type seedlings were rupted by a 70-amino-acid island between the 21st and 26 grown on medium without (þBL) or with (þBL) 10 M brassinolide. Brassinolide promotes hypocotyl elongation and retards root development in wild-type 22nd LRRs, is connected to the intracellular kinase plants but causes only mild root growth inhibition in the abs1 mutant. Scale domain through a transmembrane segment [14]. Based bar ¼ 50 mm. on the common role in BR perception, preferential con- transcript levels of the BR-downregulated Dwarf (BR C-6 servation of the functionally important extracellular oxidase) gene. Furthermore, gas-chromatography mass- regions was expected between the BRI1 proteins of dif- ferent plant species. Therefore comparing the Arabidopsis spectrometry analyses showed the accumulation of endo- [14], rice [15] and the recently available tomato and pea genous BRs, a characteristic feature of the BR-insensitive BRI1 sequences offered valuable information for identify- mutants [11,12]. Intriguingly, in spite of the nearly 30-fold ing potential ligand-binding structures. Pair-wise align- accumulation of castasterone, its immediate precursor, ments of these sequences in seven BRI1 regions (Fig. 2) BL could not be detected in the mutant samples. This revealed the highest average amino acid identity between seems to confirm the view that castasterone is a bioactive the kinase domains (83%). Somewhat surprisingly, among BR in tomato [13]. the extracellular regions, the island domain (in which the Allelism tests between the two mutants clarified that known Arabidopsis bri1 mutations are over-represented) abs1 is a new, weaker allele of cu3 [8]. Because BRI1 is was less conserved (61%) than the flanking LRRs on its thought to be the major non-redundant component of BR 2abs N-terminal (72%) and C-terminal (62%) sides. These data signalling in Arabidopsis, cu3 and cu3 plants were suggest that the LRRs around the island are crucial for assumed to carry mutations in the gene encoding tBRI1. establishing interaction with the ligand or components of Using an approach that should be useful for isolating the BR receptor complex. BRI1 homologs from various plant species, a segment of Unexpectedly, the amino acid sequence analyses led to tBRI1 was PCR-amplified from genomic DNA samples with the recognition that tBRI1 is
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