systemin and brassinolide

Small signaling molecules that mediate cell-cell communication are essential for developmental regulation in multicellular organisms. Among them are the steroids and peptide hormones that regulate growth in both plants and animals. In plants, brassinosteroids (BRs) are perceived by the cell surface receptor kinase BRI1, which is distinct from the animal steroid receptors. Identification of components of the BR signaling pathway has revealed similarities to other animal and plant signal transduction pathways. Recent studies demonstrated that tomato BRI1 (tBRI1) perceives both BR and the peptide hormone systemin, raising new questions about the molecular mechanism and evolution of receptor-ligand specificity.

Topics: Brassinosteroids; Cholestanols; Ligands; Peptides; Plant Growth Regulators; Protein Kinases; Receptors, Cell Surface; Receptors, Steroid; Signal Transduction; Solanum lycopersicum; Steroids, Heterocyclic

The tomato wound signal systemin is perceived by a specific high-affinity, saturable, and reversible cell surface receptor. This receptor was identified as the receptor-like kinase SR160, which turned out to be identical to the brassinosteroid receptor BRI1. Recently, it has been shown that the tomato bri1 null mutant cu3 is as sensitive to systemin as wild type plants. Here we explored these contradictory findings by studying the responses of tobacco plants (Nicotiana tabacum) to systemin. A fluorescently-labeled systemin analog bound specifically to plasma membranes of tobacco suspension-cultured cells that expressed the tomato BRI1-FLAG transgene, but not to wild type tobacco cells. On the other hand, signaling responses to systemin, such as activation of mitogen-activated protein kinases and medium alkalinization, were neither increased in BRI1-FLAG-overexpressing tobacco cells nor decreased in BRI1-silenced cells as compared to levels in untransformed control cells. Furthermore, in transgenic tobacco plants BRI1-FLAG became phosphorylated on threonine residues in response to brassinolide application, but not in response to systemin. When BRI1 transcript levels were reduced by virus-induced gene silencing in tomato plants, the silenced plants displayed a phenotype characteristic of bri1 mutants. However, their response to overexpression of the Prosystemin transgene was the same as in control plants. Taken together, our data suggest that BRI1 can function as a systemin binding protein, but that binding of the ligand does not transduce the signal into the cell. This unusual behavior and the nature of the elusive systemin receptor will be discussed.

Topics: Amino Acid Sequence; Brassinosteroids; Cell Membrane; Cells, Cultured; Cholestanols; Fluorescent Dyes; Gene Silencing; Immunoblotting; Immunoprecipitation; Microscopy, Fluorescence; Molecular Sequence Data; Nicotiana; Peptides; Phosphorylation; Plant Proteins; Plants, Genetically Modified; Protein Binding; Protein Kinases; Reverse Transcriptase Polymerase Chain Reaction; Signal Transduction; Solanum lycopersicum; Steroids, Heterocyclic; Threonine

The tomato Leu-rich repeat receptor kinase BRASSINOSTEROID INSENSITIVE1 (BRI1) has been implicated in both peptide (systemin) and steroid (brassinosteroid [BR]) hormone perception. In an attempt to dissect these signaling pathways, we show that transgenic expression of BRI1 can restore the dwarf phenotype of the tomato curl3 (cu3) mutation. Confirmation that BRI1 is involved in BR signaling is highlighted by the lack of BR binding to microsomal fractions made from cu3 mutants and the restoration of BR responsiveness following transformation with BRI1. In addition, wound and systemin responses in the cu3 mutants are functional, as assayed by proteinase inhibitor gene induction and rapid alkalinization of culture medium. However, we observed BRI1-dependent root elongation in response to systemin in Solanum pimpinellifolium. In addition, ethylene perception is required for normal systemin responses in roots. These data taken together suggest that cu3 is not defective in systemin-induced wound signaling and that systemin perception can occur via a non-BRI1 mechanism.

Topics: Alkalies; Arabidopsis; Brassinosteroids; Cholestanols; Gene Expression Regulation, Plant; Genetic Complementation Test; Microsomes; Molecular Sequence Data; Mutation; Peptides; Phenotype; Plant Proteins; Plant Roots; Signal Transduction; Solanum; Solanum lycopersicum; Steroids, Heterocyclic; Transcriptional Activation

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 membrane-localized 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.

Topics: Animals; Brassinosteroids; Cholestanols; Conserved Sequence; Immunity, Innate; Insecta; Mutation; Peptides; Plant Diseases; Plant Growth Regulators; Protein Kinases; Receptors, Cell Surface; Signal Transduction; Solanum lycopersicum; Steroids, Heterocyclic

Brassinosteroids (BRs) are plant steroid hormones that are essential for normal plant development. To gain better understanding of the conservation of BR signaling, the partially BR-insensitive tomato mutant altered brassinolide sensitivity1 (abs1) was identified and found to be a weak allele at the curl3 (cu3) locus. BR content is increased in both of these mutants and is associated with increased expression of DWARF: The tomato homolog of the Arabidopsis Brassinosteroid Insensitive1 Leu-rich repeat (LRR) receptor-like kinase, named tBri1, was isolated using degenerate primers. Sequence analysis of tBRI1 in the mutants cu3 and abs1 revealed that cu3 is a nonsense mutant and that abs1 is a missense mutant. A comparison of BRI1 homolog sequences highlights conserved features of BRI1 sequences, with the LRRs in close proximity to the island domain showing more conservation than N-terminal LRRs. The most homologous sequences were found in the kinase and transmembrane regions. tBRI1 (SR160) also has been isolated as the putative receptor for systemin, a plant peptide hormone. This finding suggests a possible dual role for tBRI1 in steroid hormone and peptide hormone signaling.

Topics: Alleles; Amino Acid Sequence; Arabidopsis; Arabidopsis Proteins; Brassinosteroids; Cholestanols; Cloning, Molecular; Codon, Nonsense; Molecular Sequence Data; Mutation, Missense; Peptides; Phenotype; Phytosterols; Plant Growth Regulators; Plant Proteins; Protein Kinases; Receptor Protein-Tyrosine Kinases; Repetitive Sequences, Amino Acid; Sequence Homology, Amino Acid; Signal Transduction; Solanum lycopersicum; Steroids, Heterocyclic