Heat Shock-Induced Accumulation of the Glycogen Synthase Kinase 3-Like Kinase BRASSINOSTEROID INSENSITIVE 2 Promotes Early Flowering but Reduces Thermotolerance in Arabidopsis

Abstract

Brassinosteroids (BRs) are essential plant growth- and development-regulating phytohormones. When applied exogenously, BRs ameliorate heat shock (HS)-induced cell damage and enhance plant thermotolerance; however, the molecular mechanism by which BRs regulate plant thermotolerance is unknown. In this study, by analyzing the thermotolerance of a series of BR signaling mutants and plants that overexpressed different BR signaling components, we obtained comprehensive data showing that BRASSINOSTEROID INSENSITIVE 2 (BIN2) plays a major role in mediating the crosstalk between BR signaling and plant HS responses. By RNA-Seq, 608 HS- and BIN2-regulated genes were identified. An analysis of the 1-kb promoter sequences of these genes showed enrichment of an abscisic acid (ABA) INSENSITIVE 5 (ABI5)-binding cis-element. Physiological studies showed that thermotolerance was reduced in bin2-1 mutant and ABI5-OX plants but increased in the abi5 mutant, and that the abi5 mutation could recover the thermotolerance of bin2-1 plants to a wild-type level, suggesting that ABI5 functions downstream of BIN2 in regulating plant thermotolerance. Further, HS treatment increased the cellular abundance of BIN2. Both bin2-1 mutant and BIN2-OX plants showed early flowering, while the BIN2 loss-of-function mutant bin2-3 bil1 bil2 flowered late. Given these findings, we propose that under HS conditions plants increase BIN2 activity to promote early flowering and ensure species survival; however, this reduces the thermotolerance and survivability of individual plants partially by activating ABI5.

Phytochrome B enhances seed germination tolerance to high temperature by reducing S‐nitrosylation of HFR1

“…Meanwhile, previous study showed that NO causes the S ‐nitrosylation of ABI5, leading to the degradation of ABI5 during seed germination by recruiting CUL4 and KEG E3 ligase complexes (Albertos et al , 2015). However, HT induced the accumulation of ABI5 (Ren et al , 2022), and ABI5 can bind to the promoter of SOM to activate SOM expression (Lim et al , 2013). Simultaneously, HT induced the overaccumulation of NO and its metabolic SNO derivatives.…”

ERF49 mediates brassinosteroid regulation of heat stress tolerance in Arabidopsis thaliana

“…When BRs are absent, the GSK3-like kinase BIN2 (BRASSINOSTEROID INSENSITIVE 2) phosphorylates BES1 and BZR1 proteins and inactivates these two factors [ 16 ]. Recent studies reported that the addition of BR increased the thermotolerance of Arabidopsis , and BRASSINOSTEROID INSENSITIVE 2 (BIN2) plays a critical role in the regulation of plant heat stress responses [ 42 ]. The BES1, as a transcription regulator, can be dephosphorylated and directly bind to heat shock element of heat stress transcription factors to regulate the expression of HSFs to respond to heat shock [ 43 ].…”

Brassinosteroids enhance BES1‐required thermomemory in Arabidopsis thaliana

“…BRs control responses to various biotic and abiotic stress in a complex manner (T. M. Nolan et al, 2019). On the one hand, exogenous application of BR can improve the resistance of plants to several stress (Ajguz & Hayat, 2009; Albertos et al, 2022; Ren et al, 2022; Samakovli et al, 2020; Yin et al, 2018). Another hand, BR deficient and insensitive mutants revealed elevated survival rate in the face of stresses such as drought and salt stress (Divi et al, 2015; Nawaz et al, 2017; Trevor et al, 2017).…”