The production of H2O2 is critical for brassinosteroid (BR)- and abscisic acid (ABA)-induced stress tolerance in plants. In this study, the relationship between BR and ABA in the induction of H2O2 production and their roles in response to heat and paraquat (PQ) oxidative stresses were studied in tomato. Both BR and ABA induced increases in RBOH1 gene expression, NADPH oxidase activity, apoplastic H2O2 accumulation, and heat and PQ stress tolerance in wild-type plants. BR could only induced transient increases in these responses in the ABA biosynthetic mutant notabilis (not), whereas ABA induced strong and prolonged increases in these responses in the BR biosynthetic mutant d (^im) compared with wild-type plants. ABA levels were reduced in the BR biosynthetic mutant but could be elevated by exogenous BR. Silencing of RBOH1 compromised BR-induced apoplastic H2O2 production, ABA accumulation, and PQ stress responses; however, ABA-induced PQ stress responses were largely unchanged in the RBOH1-silenced plants. BR induces stress tolerance involving a positive feedback mechanism in which BR induces a rapid and transient H2O2 production by NADPH oxidase. The process in turn triggers increased ABA biosynthesis, leading to further increases in H2O2 production and prolonged stress tolerance. ABA induces H2O2 production in both the apoplastic and chloroplastic compartments.

BRASSINAZOLE RESISTANT 1 (BZR1), the critical regulator of brassinosteroid (BR) response, participates in various BR-mediated developmental processes. However, the roles of BZR1 in stress tolerance are less clear. Here, we found that BZR1-like protein in tomato controls BR response and is involved in thermotolerance by regulating the FERONIA (FER) homologs. The CRISPR-bzr1 mutant showed reduced growth and was not responsive to 24-epibrassinolide (EBR) with regard to the promotion of plant growth. Mutation in BZR1 impaired the induction of RESPIRATORY BURST OXIDASE HOMOLOG1 (RBOH1), production of H₂O₂ in the apoplast and heat tolerance. Exogenous H₂O₂ recovered the heat tolerance of the tomato bzr1 mutant. Overexpression of BZR1 enhanced the production of apoplastic H₂O₂ and heat stress responses. However, silencing of RBOH1 abolished the BZR1-mediated heat tolerance. Further analysis showed that BZR1 bound to the promoters of FERONIA2 (FER2) and FER3 and induced their expression. Silencing of FER2/3 suppressed BZR1-dependent BR signaling for the induction of RBOH1 transcripts, accumulation of apoplastic H₂O₂ and heat tolerance. These results indicate that BZR1 regulates heat stress responses in tomato through RBOH1-dependent reactive oxygen species (ROS) signaling, which is at least partially mediated by FER2 and FER3.

Significance: For almost a century, auxin had been well-known as the master regulator of apical dominance. Recently, however, sugars were shown to be the initial regulator of apical dominance, while strigolactones (SLs) and cytokinins (CKs) act downstream of auxin to control bud outgrowth. However, the interactions of the different pathways have remained outstanding questions. Here, we report that brassinosteroids (BRs) are essential for the release of apical dominance in tomato. CK signaling relays information from auxin, SL, and sugars to promote the production of BRs, which activate the BZR1 transcription factor to suppress the expression of BRANCHED1 , an inhibitor of bud outgrowth. These findings demonstrate that hormonal and metabolic pathways impinge on a common BR signaling for controlling shoot branching.

Brassinosteroids (BRs) and abscisic acid (ABA) are essential regulators of plant growth and stress tolerance. Although the antagonistic interaction of BRs and ABA is proposed to ensure the balance between growth and defense in model plants, the crosstalk between BRs and ABA in response to chilling in tomato (Solanum lycopersicum), a warm‐climate horticultural crop, is unclear. Here, we determined that overexpression of the BR biosynthesis gene DWARF (DWF) or the key BR signaling gene BRASSINAZOLE‐RESISTANT1 (BZR1) increases ABA levels in response to chilling stress via positively regulating the expression of the ABA biosynthesis gene 9‐CIS‐EPOXYCAROTENOID DIOXYGENASE1 (NCED1). BR‐induced chilling tolerance was mostly dependent on ABA biosynthesis. Chilling stress or high BR levels decreased the abundance of BRASSINOSTEROID‐INSENSITIVE2 (BIN2), a negative regulator of BR signaling. Moreover, we observed that chilling stress increases BR levels and results in the accumulation of BZR1. BIN2 negatively regulated both the accumulation of BZR1 protein and chilling tolerance by suppressing ABA biosynthesis. Our results demonstrate that BR signaling positively regulates chilling tolerance via ABA biosynthesis in tomato. The study has implications in production of warm‐climate crops in horticulture.