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Review
. 2020 Jul 20;21(14):5108.
doi: 10.3390/ijms21145108.

Linking Brassinosteroid and ABA Signaling in the Context of Stress Acclimation

Victor P Bulgakov  1 , Tatiana V Avramenko  1   2
Affiliations
Review

Linking Brassinosteroid and ABA Signaling in the Context of Stress Acclimation

Victor P Bulgakov et al. Int J Mol Sci. .

Abstract

The important regulatory role of brassinosteroids (BRs) in the mechanisms of tolerance to multiple stresses is well known. Growing data indicate that the phenomenon of BR-mediated drought stress tolerance can be explained by the generation of stress memory (the process known as 'priming' or 'acclimation'). In this review, we summarize the data on BR and abscisic acid (ABA) signaling to show the interconnection between the pathways in the stress memory acquisition. Starting from brassinosteroid receptors brassinosteroid insensitive 1 (BRI1) and receptor-like protein kinase BRI1-like 3 (BRL3) and propagating through BR-signaling kinases 1 and 3 (BSK1/3) → BRI1 suppressor 1 (BSU1) -‖ brassinosteroid insensitive 2 (BIN2) pathway, BR and ABA signaling are linked through BIN2 kinase. Bioinformatics data suggest possible modules by which BRs can affect the memory to drought or cold stresses. These are the BIN2 → SNF1-related protein kinases (SnRK2s) → abscisic acid responsive elements-binding factor 2 (ABF2) module; BRI1-EMS-supressor 1 (BES1) or brassinazole-resistant 1 protein (BZR1)-TOPLESS (TPL)-histone deacetylase 19 (HDA19) repressor complexes, and the BZR1/BES1 → flowering locus C (FLC)/flowering time control protein FCA (FCA) pathway. Acclimation processes can be also regulated by BR signaling associated with stress reactions caused by an accumulation of misfolded proteins in the endoplasmic reticulum.

Keywords: ABA signaling; brassinosteroid signaling cascade; drought tolerance; priming; stress adaptation; stress memory.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
The pathway of BRL3 signaling. Brassinosteroid receptors BRL1, BRL3, and BRI1/BAK1 trigger the BR signaling pathway (proteins of the BR signaling system are shown in gray). BRL2 is not connected to this system. Solid lines represent protein–protein interactions presented in PAIR, IntAct, and BioGRID, and dashed lines represent possible interactions taken from STRING. Dotted lines represent transcriptional regulation. Green lines indicate signaling in the module BRL3 → BSK1/3 → BSU1 ―‖ BIN2. BIN2 regulates expression of BZR1 and BES1. BIN2 regulates drought tolerance directly by activating RD26, indirectly via BZR1-DREB1B and SnRK2.2/2.3-ABF2-DREB2A pathways. BIN2 also interacts with ICE1, implementing time-dependent regulation of the SnRK2.6/OST1-HOS1-ICE1 cold signaling module. Finally, BIN2 activates ABI5, an important concentrator of ABA signals. Red protein labels indicate that these proteins are involved in stress memory generation. These interactions were visualized using the program Cytoscape as described previously [27]. The data loaded into the program were obtained from PAIR version 3.3 [http://www.cls.zju.edu.cn/pair/]. The protein–protein interactions presented in PAIR were supplemented with data from BioGRID [http://thebiogrid.org/], UniProtKB [https://www.uniprot.org/], TAIR [https://www.arabidopsis.org/], IntAct [https://www.ebi.ac.uk/intact/interactors/], and STRING [https://string-db.org/] databases. Abbreviations: ABI1/3/5, ABA insensitive 1/3/5; ABF2, abscisic acid responsive elements-binding factor 2; BAK1, BRI1-associated receptor serine/threonine kinase; BES1, brassinazole-resistant 2; BIN2, brassinosteroid insensitive 2; BRI1, brassinosteroid insensitive 1; BRL1/2/3, serine/threonine-protein kinase BRI1-like 1/2/3; BSK1/3, BR-signaling kinases 1 and 3; BSU1, BRI1 suppressor 1; BZR1, brassinazole-resistant 1; CDPK6 and CPK32, calcium-dependent protein kinases; DREB1B,1C,2A, dehydration-responsive element-binding proteins; FCA, flowering time control protein; FLC, flowering locus C; FLS2, LRR receptor-like serine/threonine-protein kinase; GSK1, shaggy-related protein kinase iota; HDA19, histone deacetylase 19; HOS1, E3 ubiquitin-protein ligase HOS1; HSFs, heat shock factors; ICE1, inducer of CBP expression 1; RD26, NAC transcription factor; TPL, TOPLESS; SnRK2.2/2.3, SNF1-related protein kinases 2.2 and 2.3; VHA-A2, vacuolar proton ATPase.
Figure 2
Figure 2
A model of stress memory generation by BR signaling. Solid lines represent protein–protein interactions and dotted lines represent transcriptional regulation. Proteins, involved in stress memory generation, are FLC and FCA (which substantially reduce plant water use and are important for heat and cold adaptation), TPL/HDA19 complex (ensures the epigenetic link between BR and ABA signaling through BZR1/BES1-ABI3-ABI5 interactions), and key components of the ABA signaling system such as SnRK2.2/2.3 and OST1/SnRK2.6, ABA-responsive element binding factors ABI3, ABI5 and ABF2 (involved in abiotic stress defense and stress memory). BZR1 recognizes and binds to a BRRE cis element in FLC and recruits H3K27 demethylase to dynamically modulate plant response to BR signals and environmental cues. SWI/SNF CRC is also a possible memory generator in this scheme. HSF function in BR signaling is possible, but has not been studied. Abbreviations: ABI5, ABA insensitive 5; BES1, brassinazole-resistant 2; BIN2, brassinosteroid insensitive 2; BRI1, brassinosteroid insensitive 1; BRL3, serine/threonine-protein kinase BRI1-like 3; BSK1/3, BR-signaling kinases 1 and 3; BRM, ATP-dependent helicase BRAHMA; BSU, BRI1 suppressor 1; BZR1, brassinazole-resistant 1; SWI/SNF CRC, (Switch/Sucrose non-fermenting, ATP-dependent chromatin remodeling complex); FCA, flowering time control protein; FLC, flowering locus C; GSK1, shaggy-related protein kinase iota; HDA19, histone deacetylase 19; HSP, heat shock protein; HSF, heat shock factor; SWI3B/3C, chromatin remodeling complex subunits; SYD, SWI2/SNF2-type ATPase; TPL, TOPLESS; SnRK2s, SNF1-related protein kinases 2.
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