Abscisic Acid Signaling Inhibits Brassinosteroid Signaling through Dampening the Dephosphorylation of BIN2 by ABI1 and ABI2

Abstract

Abscisic acid (ABA) and brassinosteroid (BR) antagonistically regulate many aspects of plant growth and development. Previous physiological studies have revealed that the inhibition of BR signaling by ABA is largely dependent on ABI1 and ABI2. However, the genetic and molecular basis of how ABI1 and ABI2 are involved in inhibiting BR signaling remains unclear. Although it is known that in the BR signaling pathway the ABA-BR crosstalk occurs in the downstream of BR receptor complex but upstream of BIN2 kinase, a negative regulator of BR signaling, the component that acts as the hub to directly mediate their crosstalk remains a big mystery. Here, we found that ABI1 and ABI2 interact with and dephosphorylate BIN2 to regulate its activity toward the phosphorylation of BES1. By in vitro mimicking ABA signal transduction, we found that ABA can promote BIN2 phosphorylation by inhibiting ABI2 through ABA receptors. RNA-sequencing analysis further demonstrated that ABA inhibits BR signaling through the ABA primary signaling components, including its receptors and ABI2, and that ABA and GSK3s co-regulate a common set of stress-responsive genes. Because BIN2 can interact with and phosphorylate SnRK2s to activate its kinase activity, our study also reveals there is a module of PP2Cs-BIN2-SnRK2s in the ABA signaling pathway. Collectively, these findings provide significant insights into how plants balance growth and survival by coordinately regulating the growth-promoting signaling pathway and stress responses under abiotic stresses.

BES1 hinders ABSCISIC ACID INSENSITIVE5 and promotes seed germination in Arabidopsis

“…Another study demonstrated that BIN2 could also phosphorylate SnRK2.2 and SnRK2.3, which is crucial for their activity (Cai et al ., ). A new study has recently reported that ABI1/ABI2, the PP2C phosphatases of the ABA signaling pathway, could interact with and dephosphorylate BIN2 (Wang et al ., ). These studies collectively identify a new module consisting of PP2Cs‐BIN2‐SnRK2s that also links the BR and ABA signaling pathways to regulate the seed‐to‐seedling transition.…”

Brassinosteroids: Multidimensional Regulators of Plant Growth, Development, and Stress Responses

“…HISTONE DEACETYLASE6 (HDA6) deacetylates BIN2, thereby repressing its kinase activity (Hao et al, 2016), whereas BIN2 is activated via oxidation at specific Cys residues (Song et al, 2018b). Dephosphorylation by RELATED TO ABSCISIC ACID INSENSITIVE1 (ABI1) and ABI2 (which negatively regulate abscisic acid [ABA] signaling) activates BIN2 in the presence of ABA (Wang et al, 2018a;Jiang et al, 2019). These diverse regulatory mechanisms highlight the multifaceted control of BIN2 kinase activity under different conditions and in different tissues.…”

“…Because ABA production is induced during drought stress to promote stress tolerance (Cutler et al, 2010), these observations point toward a close relationship between BR and ABA pathways (Zhang et al, 2009b). Indeed, the molecular basis for BR-ABA antagonism has been extensively defined, ranging from interactions between downstream TFs such as BES1 and ABI3 or ABI5 (Ryu et al, 2014;Yang et al, 2016) to BIN2 kinase, a negative regulator of the BR signaling pathway that becomes activated in the presence of ABA (Wang et al, 2018a). BIN2 phosphorylates and promotes the activity of positive regulators in the ABA pathway including SnRK2 kinases (Cai et al, 2014) and TFs such as ABI5 (Hu and Yu, 2014).…”

Molecular Mechanisms of Brassinosteroid-Mediated Responses to Changing Environments in Arabidopsis

“…Drought is one of the most common abiotic stresses against plant growth and even survival [142]. Several studies revealed roles of BRs in plant tolerance to drought, acting mainly in crosstalk with abscisic acid (ABA) signaling [79,[143][144][145][146]. The proposed ABA signaling pathway consists of a group of ABA receptors named PYRABACTIN RESISTANCE1/PYR1-LIKE/REGULATORY COMPONENTS OF ABA RECEPTORS (PYR/PYL/RCAR), a family of type 2C PROTEIN PHOSPHATASES (PP2Cs, e.g., ABI1 and ABI2) as the coreceptors negatively regulating ABA signaling, a class of Snf1-Related Kinase 2s (SnRK2s) as positive regulators, and a class of ABA-responsive element-binding factors (ABFs) as the downstream transcription factors [147].…”

“…At the receptor level, the function of BRI1 can be post-translationally regulated by PUB12/13-directed ubiquitination, PP2A-mediated dephosphorylation, BKI1-mediated kinase inhibition, and BIK1-and BIR3-mediated competition for the coreceptor BAK1 [69][70][71][72][73]. At the BIN2 level, it has been reported that BIN2 is regulated by OCTOPUSor POLAR-mediated membrane sequestration, HDA6-mediated deacetylation, KIB1-mediated ubiquitination, TTL-enhanced interaction with BSU1, ABI1/2-mediated dephosphorylation, and ROS (reactive oxygen species)-mediated oxidation [74][75][76][77][78][79][80]. At the transcription level, it has been reported that PP2A phosphatases can promote BR signaling by dephosphorylating BES1 and BZR1, whereas 14-3-3 and BRZ-SENSITIVE-SHORT HYPOCOTYL1 (BSS1) negatively regulate BR signaling by inhibiting the translocation of BES1 and BZR1 from the cytosol to the nucleus [81][82][83].…”