Brassinosteroid signaling and molecular crosstalk with nutrients in plants

As sessile organisms, plants have to integrate hormonal signals and various nutrient stimuli to tightly adjust their growth and development in response to the changing environmental conditions. Brassinosteroids (BRs) are a group of plant steroid hormones that play critical roles in plant growth and developmental processes as well as plant responses to environmental stimuli (Nolan et al., 2020). Plants with impaired BR biosynthesis and signaling exhibit various growth defects, including de-etiolation in the dark, dwarfism, dark-green leaves, and reduced organ expansion and fertility (Clouse, 2011). Extensive studies using genetic, molecular, and biochemical approaches have characterized the BR biosynthetic pathway, and identified the core components of the BR signaling cascade from the initial receptors to the downstream transcription factors (Kim and Wang, 2010). BRs are perceived by the plasma membrane (PM)-located receptor kinase BRASSINOSTEROID INSENSITIVE1 (BRI1) and its co-receptor BRI1-ASSOCIATED KINASE1 (BAK1), which induces the transphosphorylation between BRI1 and BAK1, and thus activates BRI1 (Li and Chory, 1997; Li et al., 2002; Nam and Li, 2002). Activated BRI1 phosphorylates and activates two subclasses of receptor-like cytoplasmic kinases, the BR-SIGNALING KINASEs (BSKs) and CONSTITUTIVE DIFFERENTIAL GROWTH1 (CDG1) families of kinases (Tang et al., 2008; Kim et al., 2011). BSKs and CDG1 activate the PP1-type phosphatase BRI1-SUPPRESSOR1 (BSU1), which subsequently dephosphorylates and inactivates BRASSINOSTEROID INSENSITIVE2 (BIN2) (Kim et al., 2009; Kim et al., 2011). When the BR level is low, BIN2 is activated to phosphorylate the BRASSINAZOLE-RESISTANT1 (BZR1) and BRI1-EMS-SUPPRESSOR1 (BES1) family transcription factors, which results in the accumulation of phosphorylated BZR1/BES1 in the cytosol (Wang et al., 2002; Yin et al., 2002). When the BR level is high, BIN2 is inactivated and degraded, and BZR1 is dephosphorylated by PROTEIN PHOSPHATASE 2A (PP2A) (Tang et al., 2011; Zhu et al., 2017). Dephosphorylated BZR1 and BES1 accumulate in the nucleus and bind to the promoters of downstream BR-responsive genes to modulate their expression and regulate diverse plant growth and stress responses (Sun et al., 2010; Yu et al., 2011).

All living organisms rely on the availability of nutrients and energy to sustain cell metabolism and energy production (Rolland et al., 2006). Plants, like other eukaryotic organisms, have evolved elaborate systems for monitoring the amount of available nutrients and energy and adapting their transcriptional, translational, and metabolic responses to this information (Dobrenel et al., 2016; Li et al., 2021b). Nutrients not only serve as resources from which plants produce biomass and generate energy, but also function as signals that regulate metabolic and developmental processes, optimizing plant survival under specific nutritional conditions (Li et al., 2021b). Sugars are the primary source of carbon (C) and energy in plants, nitrogen (N), phosphorus (P), and iron (Fe) are essential elements that limit plant growth. An increasing number of experiments have indicated that nutrient-derived signals crosstalk with phytohormones to regulate plant growth and development. In this review, we summarize recent advances in the regulation of BR homeostasis in plants, the regulatory mechanisms of three key components of the BR signaling cascade, BRI1, BIN2, and BZR1/BES1, as well as highlight the findings on the crosstalk between BR and different nutrient signals, such as sugar, N, P, and Fe.

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