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Review
. 2017 Jul 27;474(16):2641-2661.
doi: 10.1042/BCJ20160633.

Cross-talk of Brassinosteroid signaling in controlling growth and stress responses

Trevor Nolan  1 , Jiani Chen  1 , Yanhai Yin  2
Affiliations
Review

Cross-talk of Brassinosteroid signaling in controlling growth and stress responses

Trevor Nolan et al. Biochem J. .

Abstract

Plants are faced with a barrage of stresses in their environment and must constantly balance their growth and survival. As such, plants have evolved complex control systems that perceive and respond to external and internal stimuli in order to optimize these responses, many of which are mediated by signaling molecules such as phytohormones. One such class of molecules called Brassinosteroids (BRs) are an important group of plant steroid hormones involved in numerous aspects of plant life including growth, development and response to various stresses. The molecular determinants of the BR signaling pathway have been extensively defined, starting with the membrane-localized receptor BRI1 and co-receptor BAK1 and ultimately culminating in the activation of BES1/BZR1 family transcription factors, which direct a transcriptional network controlling the expression of thousands of genes enabling BRs to influence growth and stress programs. Here, we highlight recent progress in understanding the relationship between the BR pathway and plant stress responses and provide an integrated view of the mechanisms mediating cross-talk between BR and stress signaling.

Keywords: Brassinosteroid; cross-talk; drought; innate immunity; plant hormones; plant signal transduction.

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Conflict of interest statement

Competing Interests

The Authors declare that there are no competing interests associated with the manuscript.

Figures

Figure 1.
Figure 1.. Overview of the BR signaling pathway.
In the absence of BR, several negative regulators (BKI1 and BIK1) act to inhibit BR signaling at BRI1/BAK1 receptors, and BIN2 phosphorylates BES1/BZR1 family transcription factors to inhibit their function through several mechanisms. BIN2 also phosphorylates other transcription factors such as PIF4, MYBL2 and HAT1 to regulate their activities. Without BR signaling, expression of BR-induced genes is relatively low, whereas BR-repressed genes are more highly expressed, leading to suppressed BR responses. When present, BRs bind to receptor BRI1 and co-receptor BAK1, which leads to the disassociation of BKI1 and BIK1 as well as phosphorylation and activation of BRI1/BAK1, which activates BSK1, CDG1 and BSU1. BSU1 then functions to inhibit BIN2 kinase function while KIB1 ubiquitinates BIN2. PP2A activates BES1/BZR1 by dephosphorylation and cytoplasmic BKI1 sequesters 14–3-3s that otherwise sequester BES1/BZR1 in the cytoplasm. These events lead to accumulation of dephosphorylated BES1/BZR1 in the nucleus. BES1/BZR1 binds to E-box elements and interacts with cofactors (such as histone-modifying enzymes REF6 and SDG8 and transcription elongation factor IWS1) and BR-related transcription factors (BR-TFs, such as PIF4 and BIM1) to activate BR-induced gene expression. On the other hand, BES1/BZR1 binds to BRRE sites and interacts with co-repressors (TPL and MYBL2), histone deacetylase (HDAC) and likely other BR-TFs to inhibit BR-repressed genes. The large number of BR-regulated genes (~5000) enables cell elongation and other BR-regulated processes.
Figure 2.
Figure 2.. Cross-talk between BR and drought pathways.
Drought induces ABA accumulation, which promotes drought responses. ABA acts through receptors (PYR/PYL/RCAR) to inhibit PP2C repression of SnRKs, allowing SnRKs to phosphorylate downstream transcription factors (ABI3/ABI5 and others), which regulate genes for drought responses. ABA-activated OST1/SnRK2.6 also functions to regulate stomatal closure. There are several mechanisms of cross-talk between drought/ABA and BR pathways that involve the negative regulator of the BR pathway BIN2 and converge on BES1/BZR1. 1. ABA induces the expression of REM4.1 through SnRK2 and bZIP28; and REM4.1 acts to inhibit BRI1/BAK1 and thus BR signaling. 2. BAK1 and ABI1/PP2C oppositely regulate OST1/SnRK2.6 to modulate stomatal closure, providing another layer to BR–ABA cross-talk. 3. Under drought conditions, BIN2 is active, which phosphorylates and activates SnRK2.2/2.3 and ABI5. 4. During stress conditions, BES1 is ubiquitinated by SINAT E3 ubiquitin ligases and targeted for degradation through selective autophagy via phospho-regulated autophagy receptor DSK2. Phosphorylation of DSK2 by BIN2 enhances DSK2–ATG8 interactions, therefore promoting BES1 degradation. 5. Drought and ABA activate NAC family transcription factor RD26 that inhibits BES1 activity to promote drought-induced (BR-repressed) genes and inhibit drought-repressed (BR-induced) genes. 6. In contrast, under BR-promoted growth conditions, BRI1 phosphorylates and inactivates REM4.1. 7. BR-activated BES1/BZR1 inhibits ABI5 expression to inhibit ABA responses either through ABI3 (top) or by directly binding ABI5 promoter (bottom). 8. On the other hand, BES1 also inhibits RD26 transcriptional activity to promote BR-induced (drought-repressed) genes and inhibit drought-induced (BR-repressed) genes, thereby promoting BR-regulated growth.
Figure 3.
Figure 3.. RD26 and BES1 regulate a common set of BR and drought genes.
(A) Comparisons of RD26 and BES1/BZR1 target genes with those regulated by RD26 OX, BRs or drought. Gene lists were obtained from previously published datasets [7,44,45,49,112,121] and statistical significance of their intersection was assessed using Fisher’s exact test. Color legend indicates −log10 transformed P-values for the intersection between the given pair of genes; black boxes indicate the total number of genes in each list. (B) Venn diagram showing a core set of 594 genes that are both BES1/BZR1 and RD26 targets and regulated in RD26OX as well as by BRs and drought. (C) The G-box motif is enriched in the core set of genes shown in (B) in DREME promoter motif analysis [171] (left), which supports a model in which BES1 and RD26 bind to a common promoter element to inhibit each other’s function (right). (D) Clustering analysis of BR-responsive gene expression for 594 core genes from (B) using published RD26 OX and rd26q RNA-seq data [112], showing that these genes are strongly influenced by RD26.
Figure 4.
Figure 4.. Cross-talk between BR and immunity.
There is multi-layer cross-talk between BR and plant immunity pathways. 1. Genetic studies indicated that BR and PAMP receptors may compete for common co-receptor BAK1, thus enabling BR repression of PTI. 2. Bacterial infection leads to phosphorylation and activation of BIK1, which activates RBOH and ROS burst to confer hypersensitive response. 3. In the nucleus, BR-activated BZR1 can inhibit PTI-mediated defense gene expression through WRKY11/15/18, HBI1 or in collaboration with WRKY40. 4. BZR1 can also function through JA and GA pathways (directly or through NAC transcription factor JUB1) to regulate fungal defense. 5. JUB1 can modulate BR and SA pathways to inhibit bacterial defense. 6. In contrast, BES1 is activated by the MAPK pathway and plays a positive role in bacterial defense, which involves MYB30, its E3 ligase MIEL1 and likely other regulators. 7. Recent studies also suggest that BR signals to activate MEK2–SIPK through BRI1 and BSK1, which in turn triggers RBOH to generate ROS to confer virus resistance. On the other branch, BES1 inhibits the expression of RBOH and thus virus resistance, mediating tradeoffs between BES1-promoted growth and virus resistance.
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