Q&A: what are brassinosteroids and how do they act in plants?
© The Author(s). 2016
Published: 22 December 2016
Brassinosteroids (BRs) are a class of polyhydroxylated steroidal phytohormones in plants with similar structures to animals’ steroid hormones. Brassinosteroids regulate a wide range of physiological processes including plant growth, development and immunity. Brassinosteroid signalling and its integration with other signalling pathways have been investigated thoroughly at the molecular level.
What are the plant steroid hormones brassinosteroids?
Brasinosteroids, defined as the sixth plant hormone after the classic plant hormones auxin, gibberellins, cytokinin, abscisic acid and ethylene, are analogous to animal steroid hormones in structure [1, 2]. Similar to animal hormones, brassinosteroids play crucial roles in diverse aspects of plant biology, including cell elongation, cell division, root growth, photo-morphogenesis, stomatal and vascular differentiation, seed germination, immunity and reproduction [3, 4]. Brassinosteroids are also involved in regulating the metabolism of plant oxidation radicals, ethylene synthesis and root gravitropic response, and have a role in mediating plant responses to stress, such as freezing, drought, salinity, disease, heat and nutrient deficiency [5–7]. This subfamily of hormones regulates a broad range of processes in plant development and responses to environmental stresses, and their analogs have been shown to bring substantial increases in grain yield, depending on growth status.
How were brassinosteroids found?
Mitchell and co-workers extracted specific ingredients with growth-promoting activity from Brassica pollen after screening nearly 60 species of plants. Histological analysis showed that the reactions induced by these ingredients were different from those induced by gibberellins . They therefore speculated that these ingredients were a new class of hormones, termed brassins. This hypothesis, however, was not accepted by some other researchers, who argued that the physiological activities of the ingredients could have been caused by gibberellin due to the crude nature of the extract from which brassins were identified . Given the potential applications of brassins in agriculture, efforts organized by the US Department of Agriculture led to purification of 4 mg of brassins from 500 pounds of bee-collected Brassica pollen. The crystal structure of the purified brassins was then solved and brassinolide was identified as the active component . These findings marked the discovery of the first plant steroidal hormone. Currently, nearly 70 kinds of natural brassinolide analogues have been isolated from tissues of various plant species, which compose the new class of plant hormone, BRs .
What are the structures of brassinosteroids?
What parts of plants are brassinosteroids usually found in?
Brassinosteroids have been found in various species of plants, including monoplast freshwater algae and brown algae, indicating that BRs are a widespread ancient plant hormone . Distributions of BRs differ among distinct tissues of individual species. Pollens, immature seeds, roots and flowers were found to have the highest content, ranging from 1–100 ng/g fw (fresh weight), while shoots and leaves have lower amounts 0.01–0.1 ng/g fw . The content and distributions of different BR analogues also vary among tissues. Unlike other hormones, endogenous BRs do not move between tissues but function in a paracrine or autocrine way as demonstrated by grafting experiments using a BR-deficient mutant of pea [14, 15]. One reason for this is likely that BR biosynthesis genes are widespread in various tissues of plant and BRs can be synthesized in situ. Long-distance effects of BRs depend on their crosstalk with other hormones like auxins and gibberellin . However, BRs need transporting from their synthesis sites in the ER to the plasma membrane and early endosomal compartments where they are perceived through passive or active intracellular transport.
What do plants do with excess brassinosteroids?
Plants synthesize BRs continuously to meet their need for growth and development, but excess BRs can be metabolized rapidly, as demonstrated by exogenous application of BRs. BR metabolism can be classified into modification of their steroidal skeletons and modification of their side chains . A number of reactions, such as dehydrogenation, demethylation, epimerization, esterification, glycosylation, hydroxylation, side-chain cleavage and sulfonation, have been found to inactivate BRs, though the mechanisms underlying this remain unclear. It has been suggested that inactive BRs can be converted into active forms to maintain BR homeostasis [12, 18].
What are the receptors for brassinosteroids?
Studies from several laboratories contributed to the finding of the first BR receptor . Clouse et al. identified the first BR-insensitive (BRI) mutant (named bri1) by observing the promotion of root elongation under inhibitory concentrations of BR compared to the wild type in Arabidopsis . The bri1 mutant displayed dwarfism, reduced cell elongation, dark-green and thickened leaves, reduced apical dominance, delayed blooming and senescence, altered vascular patterning and male sterility. The positional cloning of BRI1 was performed by Jianming Li and J. Chory, who identified 18 alleles of bri1. Despite structural similarity between BRs and animal steroid hormones, BRI1 does not structurally resemble the nuclear steroid receptors of animals but encodes a leucine-rich repeat receptor-like kinase (LRR-RLK) with an extracellular leucine-rich repeat (LRR) domain and an intracellular serine/threonine kinase domain . BRI1 is highly conserved across different plant species , consistent with the finding that BRs are widely present in plants. There are three BRI1 homologues in Arabidopsis, BRL1, BRL2 and BRL3. BRL1 and BRL3, but not BRL2, were shown to bind BRs with high affinity and rescue the phenotypes of the BRI1 mutation when expressed using the promoter of BRI1 . Thus far, the ligands BRL2 might recognize still remain unknown. BRI1 is highly expressed in various tissues of plants and functions as the major receptor of BRs, whereas the expression of BRL1 and BRL3 is confined to vascular cells and display weak phenotypes when knocked out .
What are the BRI1-associated receptor kinases?
In 2002, J.C. Walker’s group, using a bri1 suppressor screen, and Jianming Li’s group, using a yeast two-hybrid screen, independently found a BRI1-interacting partner, an LRR-RLK named BRI1-associated kinase 1 (BAK1). Both groups presented evidence showing that BRI1 and BAK1 interacted with each other in vitro and in vivo, which contributed to BR signalling [23, 24]. BAK1 is also called SERK3, as it belongs to the family of SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASEs (SERKs), of which there are five members (SERK1–SERK5) in Arabidopsis . Later on, SERK1 and SERK4 were shown to have a similar role to BAK1/SERK3 in BR-induced signalling [26, 27]. The serk1 bak1 bkk1 triple null mutant phenocopied a null bri1 mutant, establishing an indispensable role of SERKs in BR signalling .
How does BRI1 recognize brassinosteroids and consequently become activated?
How are the signals downstream of brassinosteroid signalling transduced?
The potential role of brassinosteroids in the plant growth-immunity trade-off is intriguing—can you describe it?
Brassinosteroids regulate many development processes in plants, as well as responses to environmental stresses and their roles in the growth–defence trade-off have profound implications in agriculture and natural ecosystems. To ensure perpetuation, plants need to balance their limited resources for growth and defence . Several plant hormones, including BRs, have been suggested to play roles in the trade-off between growth and defence . Recent studies indicated that interaction of BR signalling with PAMP-triggered immunity is unidirectional and negative [43, 44]. More recent data appear to support the idea that the interaction is located at the transcriptional level rather than at the receptor complex [45–48], though the underlying mechanisms remain debatable. Understanding of the mechanisms for these trade-offs is expected to provide a foundation for development of breeding strategies to maximize crop yield.
What other unknowns are there in brassinosteroid signalling?
Great advances have been achieved in our understanding of the BR signalling pathway and BR biosynthesis and metabolism. However, it remains unclear how brassinosteroid-induced BRI1-BAK1 heterodimerization activates the kinase activity of BRI1. Fully addressing this question will require detailed elucidation of structure of the full-length complex. New components are being identified in brassinosteroid signalling and understanding of how they are integrated with other signalling pathways will be important to gain a comprehensive and systematic view of brassinosteroid functions in various plants [49, 50]. A full elucidation of brassinosteroid signalling events and their integration with other signalling pathways will enable brassinosteroid to be applied in agriculture.
JC is supported by grants from Projects of International Cooperation and Exchanges NSFC (31420103906), National Natural Science Foundation of China (31130063 and 31421001), and Chinese Ministry of Science and Technology (2015CB910200).
The authors declare that they have no competing interests.
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