The brassinosteroid signaling pathway-new key players and interconnections with other signaling networks crucial for plant development and stress tolerance

Abstract

Brassinosteroids (BRs) are a class of steroid hormones regulating a wide range of physiological processes during the plant life cycle from seed development to the modulation of flowering and senescence. The last decades, and recent years in particular, have witnessed a significant advance in the elucidation of the molecular mechanisms of BR signaling from perception by the transmembrane receptor complex to the regulation of transcription factors influencing expression of the target genes. Application of the new approaches shed light on the molecular functions of the key players regulating the BR signaling cascade and allowed identification of new factors. Recent studies clearly indicated that some of the components of BR signaling pathway act as multifunctional proteins involved in other signaling networks regulating diverse physiological processes, such as photomorphogenesis, cell death control, stomatal development, flowering, plant immunity to pathogens and metabolic responses to stress conditions, including salinity. Regulation of some of these processes is mediated through a crosstalk between BR signalosome and the signaling cascades of other hormones, including auxin, abscisic acid, ethylene and salicylic acid. Unravelling the complicated mechanisms of BR signaling and its interconnections with other molecular networks may be of great importance for future practical applications in agriculture.

Figure 1

Pattern of auto- and transphosphorylation sites of the BRI1 and BAK1 proteins. Autophosphorylation sites are shown as squares, whereas transphosphrylation sites as solid circles containing the letter ‘P’. Green symbols represent residues, whose phosphorylation has stimulatory effect on the activity of the BRI1 and BAK1 proteins, whereas red symbols denote phosphorylated residues with inhibitory impact on the activity of the BRI1-BAK1 receptor complex. Abbreviations: TM—transmembrane domain, JM—juxtamembrane region, KD—kinase domain, AL—activation loop, CTD—C-terminal domain.

Figure 2

Model of BR perception and signaling pathway. (a) In the absence of BR, formation of the receptor complex is inhibited by the C-terminal domain (CTD) of BRI1 kinase and by the BKI1 protein. Positive regulators of BR signaling are inactive, whereas the cytoplasmic BIN2 kinase phosphorylates and inactivates transcription factors, what results in their cytoplasmic retention, export for nucleus and degradation. Expression of the BR-responsive genes is repressed; (b) After BR perception by the BRI1 kinase the transmembrane receptor complex is formed and phosphorylation/dephosphorylation cascade is initiated. BIN2 kinase is inhibited, what results in accumulation of active, dephosphorylated forms of transcription factors in the nucleus and stimulation of the expression of BR-responsive genes. The green arrows denote activation, whereas the red arrows denote inhibition; ‘P’ denotes phosphorylation/dephosphorylation, whereas ‘Me’ stands for methylation.

Figure 2

Model of BR perception and signaling pathway. (a) In the absence of BR, formation of the receptor complex is inhibited by the C-terminal domain (CTD) of BRI1 kinase and by the BKI1 protein. Positive regulators of BR signaling are inactive, whereas the cytoplasmic BIN2 kinase phosphorylates and inactivates transcription factors, what results in their cytoplasmic retention, export for nucleus and degradation. Expression of the BR-responsive genes is repressed; (b) After BR perception by the BRI1 kinase the transmembrane receptor complex is formed and phosphorylation/dephosphorylation cascade is initiated. BIN2 kinase is inhibited, what results in accumulation of active, dephosphorylated forms of transcription factors in the nucleus and stimulation of the expression of BR-responsive genes. The green arrows denote activation, whereas the red arrows denote inhibition; ‘P’ denotes phosphorylation/dephosphorylation, whereas ‘Me’ stands for methylation.

Figure 3

Model of BR-dependent regulation of target gene expression, mediated by the network of transcription factors. The names of the BR-regulated genes and gene groups are italicized and shown in the blue rectangles. Green arrows show positive regulation, whereas red arrows denote repression. Black arrow indicates that function of BIN2-mediated phosphorylation of the AIFs transcription factors is currently unknown; ‘P’ denotes phosphorylation events.