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Update 102 TRENDS in Plant Science 10 Voesenek, L.A.C.J. et al. (1999) A lack of aerenchyma and high rates of radial oxygen loss from the root base contribute to the waterlogging intolerance of Brassica napus. Aust. J. Plant Physiol. 26, 87 – 93 11 Dolferus, R. et al. (1994) Differential interactions of promoter elements in stress responses of the Arabidopsis Adh gene. Plant Physiol. 105, 1075 – 1087 12 Harmer, S.L. et al. (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110 – 2113 13 Brazma, A. et al. (1996) Discovering patterns and subfamilies in biosequences. Proceedings of the Fourth International Conference on Intelligent Systems for Molecular Biology, pp. 33 – 43, AAAI Press 14 Bailey, T.L. and Elkan, C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology, pp. 28 – 36, AAAI Press 15 Thijs, G. et al. (2002) A Gibbs sampling method to detect overrepresented motifs in upstream regions of coexpressed genes. J. Comput. Biol. 9, 447 – 464 16 Spellman, P.T. et al. (1998) Comprehensive identification of cell cycleregulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell 9, 3273 – 3297 17 Bussemaker, H.J. et al. (2001) Regulatory element detection using correlation with expression. Nat. Genet. 27, 167– 171 18 Wasserman, W.W. and Fickett, J.W. (1998) Identification of regulatory Vol.8 No.3 March 2003 19 20 21 22 23 24 25 26 27 28 regions which confer muscle-specific gene expression. J. Mol. Biol. 278, 167–181 Kauffman, S.A. (1969) Homeostasis and differentiation in random genetic control networks. Nature 224, 177– 178 De Jong, H. (2002) Modeling and simulation of genetic regulatory systems: a literature review. J. Comput. Biol. 9, 67– 103 Lee, T.I. et al. (2002) Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298, 799 – 804 Ernst, D. and Aarts, M. cis elements regulating gene promoters to environmental stress. In Molecular Ecotoxicology of Plants (Sandermann, H., ed.), Springer-Verlag (in press) Singh, K.B. et al. (2002) Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol. 5, 430– 436 Fransz, P.F. and de Jong, J.H. (2002) Chromatin dynamics in plants. Curr. Opin. Plant Biol. 5, 560 – 567 Llave, C. et al. (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14, 1605– 1619 Kauffman, S.A. (1993) Origins of Order –Self-Organization and Selection in Evolution, Oxford University Press Lieb, J.D. et al. (2001) Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association. Nat. Genet. 28, 327–334 Iyer, V.R. et al. (2001) Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 409, 533– 538 1360-1385/03/$ - see front matter q 2003 Elsevier Science Ltd. All rights reserved. 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, and systemin, inducing systemic wound responses to attacks by insect pests, are newly recognized plant hormones that are perceived by plasma membranelocalized leucine-rich repeat receptor kinases. The recent characterization of the brassinosteroid receptor BRI1 from tomato revealed that this protein is identical to the previously isolated SR160 systemin receptor, strongly suggesting that both brassinosteroid and systemin signalling use the same surface receptor. Brassinosteroids (BRs) are polyhydroxy-steroid phytohormones controlling important developmental functions, such as growth, photomorphogenesis, fertility, seed germination, senescence and stress tolerance [1]. Brassinolide (BL), the most active BR, was identified in 1979; several key elements of its signalling pathway have now been characterized with the help of BR-response mutants. Perception of BL by BRASSINOSTEROID INSENSITIVE 1 (BRI1), a plasma membrane-localized leucine-rich repeat (LRR) receptor kinase, probably initiates a phosphorylation cascade that deactivates the cytoplasmic GSK3/SHAGGY-like BIN2 kinase, a negative regulator of BR signalling. By phosphorylating BES1 and BZR1, two downstream components of the pathway, BIN2 can prevent their translocation to the Corresponding author: Miklos Szekeres ([email protected]). http://plants.trends.com nucleus, where they act as positive regulators of BR-responsive gene expression [2– 4]. Considerable attention has been focused on the functional characterization of BRI1, the putative BR receptor. A series of elegant experiments revealed that the extracellular portion of the protein is required for BR-dependent activation of the intracellular, Ser/Thr-specific kinase domain [5,6]. Using radiolabelled BL, it was shown that BRI1 co-immunoprecipitated with BL binding activity, but hormone binding was prevented by mutations affecting the extracellular domain of the protein [7]. These data unequivocally demonstrated that BRI1 is an essential component of the BR receptor complex. Recent cloning and sequence analysis of the tomato BRI1 gene (tBRI1) by Teresa Montoya and colleagues led to the exciting discovery that it encodes the Lycopersicon esculentum equivalent of the Lycopersicon peruvianum SR160 LRR receptor kinase [8], which had been identified as the receptor of the peptide hormone systemin [9]. Abs1 and Cu3 encode the tomato ortholog of BRI1 The BR-insensitive mutants of tomato, altered brassinolide sensitivity 1 (abs1, from L. esculentum) [8] and curl 3 (cu3, from Lycopersicon pimpinellifolium) [10] have similar phenotypic features, but abs1 is less dwarfed, develops an elongated root and retains its fertility and partial responsiveness to BL (Fig. 1). In both abs1 and cu3, reverse-transcription PCR assays detected increased Update TRENDS in Plant Science 103 Vol.8 No.3 March 2003 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 Wild type abs1 –BL +BL –BL +BL Fig. 1. Partial brassinosteroid-insensitive phenotype of the tomato (Lycopersicon esculentum) abs1 mutant. Three-week old abs1 and wild-type seedlings were grown on medium without (þBL) or with (þBL) 1026 M brassinolide. Brassinolide promotes hypocotyl elongation and retards root development in wild-type plants but causes only mild root growth inhibition in the abs1 mutant. Scale bar ¼ 50 mm. transcript levels of the BR-downregulated Dwarf (BR C-6 oxidase) gene. Furthermore, gas-chromatography massspectrometry analyses showed the accumulation of endogenous BRs, a characteristic feature of the BR-insensitive mutants [11,12]. Intriguingly, in spite of the nearly 30-fold accumulation of castasterone, its immediate precursor, BL could not be detected in the mutant samples. This seems to confirm the view that castasterone is a bioactive BR in tomato [13]. Allelism tests between the two mutants clarified that abs1 is a new, weaker allele of cu3 [8]. Because BRI1 is thought to be the major non-redundant component of BR signalling in Arabidopsis, cu3 and cu3 2abs plants were assumed to carry mutations in the gene encoding tBRI1. Using an approach that should be useful for isolating BRI1 homologs from various plant species, a segment of tBRI1 was PCR-amplified from genomic DNA samples with degenerate primers corresponding to kinase domain regions conserved in Arabidopsis and rice BRI1. Using the sequence information obtained from the PCR product, the complete tBRI1 gene could then be isolated by inverse PCR. Sequence analysis of the tBRI1 copy amplified from cu3 revealed a nonsense mutation (G749Z) in the 25th LRR motif, whereas the tBRI1 amplified from cu3 2abs identified a missense mutation (H1012Y) within the kinase domain. Co-segregation of the mutation-specific RFLP patterns with the respective BR-insensitive phenotypes confirmed that cu3 and cu3 2abs are deficient in the tomato ortholog of BRI1. http://plants.trends.com 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 sativum) [8]. The blue bars corresponding to the indicated BRI1 regions show the percentage 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 extracellular (sensor) part with 25 LRR motifs, interrupted by a 70-amino-acid island between the 21st and 22nd LRRs, is connected to the intracellular kinase domain through a transmembrane segment [14]. Based on the common role in BR perception, preferential conservation of the functionally important extracellular regions was expected between the BRI1 proteins of different plant species. Therefore comparing the Arabidopsis [14], rice [15] and the recently available tomato and pea BRI1 sequences offered valuable information for identifying potential ligand-binding structures. Pair-wise alignments of these sequences in seven BRI1 regions (Fig. 2) revealed the highest average amino acid identity between the kinase domains (83%). Somewhat surprisingly, among the extracellular regions, the island domain (in which the known Arabidopsis bri1 mutations are over-represented) was less conserved (61%) than the flanking LRRs on its N-terminal (72%) and C-terminal (62%) sides. These data suggest that the LRRs around the island are crucial for establishing interaction with the ligand or components of the BR receptor complex. Unexpectedly, the amino acid sequence analyses led to the recognition that tBRI1 is almost fully (. 99%) identical with the recently identified SR160 systemin receptor [9,16]. Because both LRR receptor kinases are encoded by singlecopy genes and their differences seem to result from interspecific variability (tBRI1 is from L. esculentum whereas SR160 is from L. peruvianum), these proteins can be regarded as each other’s functional equivalents. Tomato BRI1 can function as a dual ligand receptor Systemin is a Solanaceae family-specific peptide hormone which, following its release upon wounding, initiates systemic wound responses, partly through the induction of jasmonate synthesis [17]. Isolation of the systemin 104 Update TRENDS in Plant Science receptor was based on its high affinity toward its ligand. From a cell suspension culture that was photoaffinitylabelled with radioactive systemin, a 160-kDa plasma membrane protein was purified to homogeneity and, using its amino acid sequence, identified as the SR160 LRR receptor kinase [9]. The data presented by Montoya et al. [8] now suggest that SR160, as well as its BRI1 homolog from L. esculentum, participate in both BR and systemin signalling. This result is particularly interesting because to date only the oxytocin/progesterone receptor of mammals has been known to interact with more than one type of hormone ligand [18]. How can two phytohormones with such different structures and physiological functions be perceived by tBRI1/SR160? The binding of systemin to the receptor agrees with the anticipated role of LRRs in protein – protein interactions. By contrast, how BRs bind to the receptor is unclear. Even at high (1 mM ) concentration, BL does not compete with systemin in ligand-binding assays, indicating that BRs and systemin are perceived by different regions of the receptor, or by different binding mechanisms. For instance, it seems possible that BRI1 perceives BRs as complex ligands formed with sterolbinding proteins [19]. In such a case, this complex could compete with systemin for the receptor ligand-binding site. The questions regarding the ligand-specificity of tBRI1/SR160 remain to be elucidated by future experiments. Like other LRR receptor kinases, BRI1 is expected to function in a dimeric form: in a yeast expression system, Arabidopsis BRI1 was shown to form heterodimers and induce transphosphorylation with the structurally related Arabidopsis BAK1 receptor kinase [20,21]. Detailed molecular analyses should reveal whether BRI1-interacting kinase(s) can influence the ligand binding and kinase specificity of the receptor complex. Furthermore, studying systemin binding and signalling in BRI1-deficient tomato mutants, such as cu3 and cu3 2abs, should be instrumental in clarifying how tBRI1 can participate in both BR and systemin perception, and how tBRI1 can selectively activate the respective signalling pathways. Acknowledgements I thank Gerard Bishop for the images of tomato seedlings, as well as Éva Ádám, László Kozma-Bognár and Ferenc Nagy for helpful comments on the manuscript. Work in my laboratory is supported by the Hungarian Scientific Research Fund (Grant T 42639). References 1 Bishop, G.J. and Yokota, T. (2001) Plants steroid hormones, brassinosteroids: Current highlights of molecular aspects on their synthesis/ http://plants.trends.com Vol.8 No.3 March 2003 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 metabolism, transport, perception and response. Plant Cell Physiol. 42, 114 – 120 Clouse, S.D. (2002) Brassinosteroid signal transduction. Clarifying the pathway from ligand perception to gene expression. Mol. Cell 10, 973 – 982 Friedrichsen, D. and Chory, J. (2001) Steroid signaling in plants: from the cell surface to the nucleus. BioEssays 23, 1028 – 1036 Zhao, J. et al. (2002) Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiol. 130, 1221– 1229 He, Z.H. et al. (2000) Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288, 2360– 2363 Oh, M.H. et al. (2000) Recombinant brassinosteroid insensitive 1 receptor-like kinase autophosphorylates on serine and threonine residues and phosphorylates a conserved peptide motif in vitro. Plant Physiol. 124, 751 – 765 Wang, Z-Y. et al. (2001) BRI1 is a critical component of a plasmamembrane receptor for plant steroids. Nature 410, 380 – 383 Montoya, T. et al. (2002) Cloning the tomato Curl3 gene highlights the putative dual role of the leucine-rich repeat receptor kinase tBRI1/SR160 in plant steroid hormone and peptide hormone signaling. Plant Cell 14, 3163 – 3176 Scheer, J.M. and Ryan, C.A. Jr (2002) The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc. Natl. Acad. Sci. U. S. A. 99, 9585 – 9590 Koka, C.V. et al. (2000) A putative role for the tomato genes DUMPY and CURL3 in brassinosteroid biosynthesis and response. Plant Physiol. 122, 85 – 98 Nomura, T. et al. (1997) Blockage of brassinosteroid biosynthesis and sensitivity causes dwarfism in garden pea. Plant Physiol. 113, 31 – 37 Noguchi, T. et al. (1999) Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. Plant Physiol. 121, 743 – 752 Nomura, T. et al. (2001) Accumulation of 6-deoxocathasterone and 6-deoxocastasterone in Arabidopsis, pea and tomato is suggestive of common rate-limiting steps in brassinosteroid biosynthesis. Phytochemistry 57, 171 – 178 Li, J. and Chory, J. (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929– 938 Yamamuro, C. et al. (2000) Loss of function of a rice brassinosteroid insensitive 1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12, 1591– 1605 Yin, Y. et al. (2002) Plant receptor kinases: systemin receptor identified. Proc. Natl. Acad. Sci. U. S. A. 99, 9090 – 9092 Lindsey, K. et al. (2002) Peptides: new signalling molecules in plants. Trends Plant Sci. 7, 78 – 83 Grazzini, E. et al. (1998) Inhibition of oxytocin receptor function by direct binding of progesterone. Nature 392, 509 – 512 Bishop, G.J. and Koncz, C. (2002) Brassinosteroids and plant steroid hormone signaling. Plant Cell 14, S97 – S110 Nam, K.H. and Li, J. (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203 – 212 Li, J. et al. (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213 – 222 1360-1385/03/$ - see front matter q 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S1360-1385(03)00010-4