BRASSINOSTEROIDS: Essential Regulators of Plant Growth and DevelopmentThe interaction between brassinosteroid signaling and sucrose transport raises the brassinosteroi whether brassinosteroid and sugars jointly affect plant's innate immunity. Vesicular membrane trafficking is gaining considerable attention with regard to plant brassinosteroid review paper. The rdview here is on the subcellular compartmentation of membrane proteins involved in signaling, transport, and defense, and on the cross-talk between brassinosteroid signals and sugar availability. A direct link has been elucidated between brassinosteroid function and perception, and sucrose brassinosteroid review paper and transport. Sucrose regulation and brassinosteroid signaling cross-talk at various levels, including the well-described regulation of tren 75 gene expression: BZR-like transcription factors link the signaling pathways.
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Brassinosteroids BRs are a class of steroidal plant hormones that play diverse roles in plant growth and developmental processes. Recently, the easy availability of biological resources, and development of new molecular tools and approaches have provided the required impetus for deeper understanding of the processes involved in BRs biosynthesis, transport, signaling and degradation pathways.
From recent studies it is also evident that BRs interact with other phytohormones such as auxin, cytokinin, ethylene, gibberellin, jasmonic acid, abscisic acid, salicylic acid and polyamine in regulating wide range of physiological and developmental processes in plants. The inputs from these studies are now being linked to the versatile roles of BRs. The present review highlights the conceptual development with regard to BR homeostasis, signaling and its crosstalk with other phytohormones.
This information will assist in developing predictive models to modulate various useful traits in plants and address current challenges in agriculture. Brassinosteroids BRs are plant specific steroidal hormones, characterized by their polyhydroxylated sterol structure and were first isolated from Brassica napus pollen Grove et al.
BR are regarded as a class of essential plant hormones that plays diverse roles in monitoring broad spectrum of plant growth and developmental processes. They regulate multiple physiological functions including seed germination, cell elongation, cell division, senescence, vascular-differentiation, reproduction, root development, photomorphogenesis, and also respond to various biotic and abiotic stresses Clouse and Sasse, ; Li and Chory, ; Sreeramulu et al.
Owing to their diverse functions, extensive research has been conducted to promote BR as essential plant growth regulators for modern agriculture Ikekawa and Zhao, ; Divi and Krishna, The maintenance and regulation of endogenous level of BR is crucial for various biological functions in plants Tanaka et al.
BR biosynthesis, transport and degradation are critical components of BR homeostasis and for maintaining the endogenous level of BR in plant. It has been observed that BR-deficient mutants exhibits extreme dwarfism, altered leaf morphology, abnormal vascular development, delayed flowering and senescence, and reduced male fertility Clouse, However, excessive application of bioactive BR leads to downregulation of BR-specific biosynthesis genes and an upregulation of BR-inactivation gene, hampering normal development of plants Bishop and Yokota, ; Tanaka et al.
Moreover, a finely tuned cellular regulation of BR levels is evident from the observation that increase in endogenous BR concentration lead to feedback regulation of the BR metabolic genes, while BR deficient conditions elicit the expression of BR biosynthesis genes to maintain BR homeostasis Tanaka et al. Further to understand the BR mediated regulation of several key molecular and physiological functions in plants, extensive research have been conducted over past two decades Zhu et al.
The use of different biological approaches such as mutant screening, microarray, proteomics, protein—protein interaction studies and bioinformatics played vital role in identification and characterization of various components involved in BR signaling Divi et al.
Recent studies demonstrate that BR interacts at various level with the signaling components of other phytohormones and regulate process like plant growth and development and stress responses Hu and Yu, ; Tong et al. In the above background, the present review focuses on the recent advances in our understanding of the process of BR biosynthesis, transport, degradation and signaling.
This information is useful in getting insights into dynamics of BR homeostasis and its implication in modulating various critical functions in plants. Present update also emphasizes the interaction between the key genes and transcription factors of BR with the signaling components of other phytohormones. This information will facilitate in getting insights into a fairly complex process of BR- mediated plant responses. Model for brassinosteroid BR signaling pathway in the absence and in the presence of BR.
BR biosynthesis ensues from intricate network pathways and is mostly modulated by transcriptional regulation of BR biosynthetic genes Chung and Choe, ; Vriet et al. Various genetic and biochemical studies have elucidated BR biosynthetic pathway which commences with campesterol, a precursor for synthesis of the most active form of BR, brassinolide BL.
Firstly campesterol is converted to campestenal which was initially believed to branch into two parallel pathways, namely the early and late C-6 oxidation pathways involving a chain of reductions, hydroxylations, epimerizations and oxidations which eventually converge at castesterone that leads to the formation of BL Fujioka et al.
Later studies revealed that BR biosynthetic pathway is a triterpenoid pathway Choe, ; Chung and Choe, Mevalonic acid serves as a precursor of the triterpenoid pathway and is condensed and transformed to 2,3-oxidosqualene which further undergoes modification to form major plant sterols like sitosterols and campesterols. Depending on the availability of substrate and enzymes, campesterol can be modified by two different enzymes: Since DWF4 can act on multiple biosynthetic intermediates including campesterol and campestenol, the pathway branches to a third early C hydroxylation pathway Choe et al.
LC-MS and various genetic studies have shown that several other branches are formed by CPD, a C hydroxylase which metabolizes campesterol and other intermediates and has recently been found to participate in a C-3 oxidation as well Ohnishi et al. The intermediates formed in above mentioned reactions are further modified and later merge into late C-6 oxidation pathway thus, revealing a certain degree of crosstalk between the parallel pathways manifesting complex networking of BR biosynthesis.
Interestingly, monocots like rice and maize, lack the enzyme CYP85A2 responsible for C-6 oxidation reaction implying that BR synthesis culminates at castesterone in rice Kim et al.
Recently, it has been shown that in rice, in addition to castesterone, an alternate pathway for biosynthesis of functionally less active CBRs exists in order to increase the biological activity of BR in rice.
In contrast to other hormones, BR are not transported to long distances but are rather used in proximity to synthesizing cells. However, they undergo intracellular transport either passively or actively, from their site of synthesis in ER to the plasma membrane where its perception occurs Symons et al.
Nevertheless, BR are able to exert a long-distance effect by their crosstalk with other hormones like auxins Symons et al. The short distance transport of BR are suggested to be mediated by some carrier mechanism BR conjugates formed by binding of BR to fatty acids or glucose or through specific proteinaceous transporters Fujioka and Yokota, ; Symons et al. Several proteins belonging to the class of pathogenesis-related PR 10 family of proteins, protein family belonging to A or G classes of ABC transporters ATP binding cassette and several Sec proteins are potential candidates for mediating BR transport Markovic-Housley et al.
In the absence of a mode for long distance transport of BR, the spatial and temporal regulation of its homeostasis at the tissue or at the cellular level is extremely crucial for normal growth and development Symons et al. BR biosynthesis undergoes two-way regulation mechanism: Moreover, BR signaling mutant brassinosteroid insensitive 1 bri1 shows considerable accumulation of endogenous BR as their feedback regulation requires intact BR perception and signaling pathway Sun et al.
Evidence reveal that these conjugations may serve as temporary storage forms of pool of inactive BR and believed to serve additional functions such as irreversible inactivation, transport, compartmentalization, and protection against cellular removal Bajguz, ; Husar et al.
Recent studies have also shown that BR biosynthesis can be regulated by external stimuli like salt and temperature stress Maharjan and Choe, ; Sharma et al. In the recent past, with the use of various biochemical, genetic and proteomic approaches, a great advancement has been made in our understanding of the BR signaling pathway Zhu et al.
BRI1 and BRL1 have similar basic skeleton with 25 and 24 units of LRRs, respectively with a great degree of similarity in overall shape and curvature of the horseshoe-like structure of extracellular domain which is the seat for binding of BR.
BRL2, which is considered as another BRL1 homolog and responsible for vascular development has also been studied for its ability to bind to BR Ceserani et al. This could be due to the presence of heavily negatively charged residues located at the inner side of the binding pocket in BRL2 that result in the change in its hydrophobicity to BRs She et al. Binding of BR to the amino acids island domain of BRI1 triggers a change in the receptor either in the form of conformational change in the preformed homodimer or receptor dimerisation Wang et al.
It is hypothesized that preassembled BRI1-BAK1 after conjugation with ligand might undergo discrete rearrangements of their respective intracellular kinase domains. This hypothesis derives its significance as similar signaling paradigms is observed in receptor tyrosine kinases in animals RTKs which undergo ligand-independent receptor dimerization, followed by dimer reorganization upon ligand binding Lemmon and Schlessinger, ; Bucherl et al. Infact, BRI1 possess significant tyrosine kinase activity and it can undergo autophosphorylation on tyrosine residues within the kinase and juxtamembrane domains and can lead to transphosphorylation of Tyr in BKI1 as well as tyrosines in other proteins Oh et al.
Tyr and Tyr are identified as autophosphorylation sites in vitro and in vivo with Tyr in kinase subdomain V being essential for activity, while Tyr in the juxtamembrane domain is not essential for kinase activity but plays an important role in BR signaling in vivo Wang et al. Genome-wide protein-DNA interaction analyses as well as the expression profiling have identified about genes targeted by BZR1 downstream from the BRI1-mediated signaling pathway, while BES1 controls genes out of which a small set of genes show an overlap with the BZR1 target genes and thus regulate various genes depending on specific target gene promoter and dimerization partner Sun et al.
BR mediated regulation of gene expression involves epigenetic mechanism also. BES1 directly interacts with a pair of histone demethylases, relative of early flowering6 REF6 and its homolog ELF6 early flowering 6 belonging to the class of jumonji domain proteins, to regulate various physiological processes such as flowering time Noh et al.
BES1 can also recruit, a histone lysine methyltransferase called set domain group8 SDG8 , which is implicated in histone H3 Lys di- and trimethylation which suggests that epigenetic mechanisms are also involved in regulating the expression of a subset of BR target genes.
Recently, it has been found that BES1 physically interacts to repress transcription factor, brassinosteroids at vascular and organizing center BRAVO which acts as a cell-specific repressor of quiescent center divisions in the primary root of Arabidopsis.
Another transcription repressor, myeloblastosis family transcription factor-like 2 MYBL2 is known to interact with BES1 to down-regulate the expression of BR-repressed genes which is required for optimal BR response Ye et al.
They bind to nearly two thousand common target genes, and synergistically regulate these genes, many of which encode transcription factors and proteins that function in the cell wall and chloroplast Oh et al. HY5 is a basic leucine zipper transcription factor that functions as a positive regulator of photomorphogenesis and binds to the promoter of over a thousand genes that are also the direct targets of BZR1.
Both BZR1 and HY5 regulate the transcription of these genes in opposite ways thereby supporting an antagonistic interaction between BR and light signals Sun et al. BZS1 may also interact with Hy5 transcription factor to control expression of a subset of light-responsive genes.
BZR1 directly binds to the promoter of GATA2 to repress its function, while it is post-transcriptionally activated by light signals Luo et al. Another connection between light and BR pathways in regulating morphogenesis is provided by two related transcription factors, golden2-like 1 GLK1 and GLK2.
BES1 directly represses the expression of two related transcription factors, GLK1 and GLK2, that promote the expression of large number of photosynthetic genes and are required for chloroplast development Waters et al. Brassinosteroids perform diverse functions due to its interplay with other phytohormones. In response to environmental cues BR interact with different phytohormones such as abscisic acid ABA , auxin, cytokinin CK , ethylene, gibberellins GA , jasmonic acid JA , polyamines PA and salicylic acid SA , and to regulate myriad aspects of plant growth and developmental processes in plants Choudhary et al.
Recent studies clearly indicate that in response to various intrinsic and extrinsic factors, the signaling components of BR crosstalks with the key genes and transcription factors of other phytohormones and thereby regulates multiple functions in plants. The unraveling of these complicated mechanisms of BR signaling and its collaboration with other molecular networks will be of great importance in improving modern agriculture.
It is well documented that ABA is required to inhibit seed germination and is also mandatory to establish seed dormancy during embryo maturation. On contrary, BR promotes seed germination indicating the antagonistic interaction between both these hormones Steber and McCourt, ; Finkelstein et al. Genetic, physiological and biochemical studies have revealed that BR and ABA can co-regulate the expression of s of genes Nemhauser et al.
However, the underlying molecular mechanism and the signaling components involved in this crosstalk are largely unknown. Furthermore, BR and ABA have been suggested to play antagonistic roles in regulating seed germination and post-germinative growth processes Hu and Yu, ABA inhibits while BR-enhances seed germination and post-germinative growth processes. These results indicate that ABA biosynthesis plays a key role in sustaining stress tolerance in BR-induced pathways in plants Zhou et al.
A schematic model showing crosstalk of various pyhtohormones with brassinosteroids. Involvement of different genes and transcription factors as a key component in transcriptional regulation of plant development has been represented. Positive effects are indicated by arrows, bars indicate repression and unknown interactions are represented by dashed arrows. In ABA deficient mutant, aba , pronounced effects of BR application were observed under heat stress conditions with respect to survival rate due to higher accumulation of heat shock protein90 HSP90 , it indicates that ABA conceals the effect of BR in plant stress responses Divi et al.
It has been observed that under abiotic stress salt and drought stress and upon exogenous phytohormone application BR and ABA , the transcript levels of BSK5 gene were enhanced.
Crosstalk between BR and auxin regulates myriad aspects of plant growth and developmental processes, Hao et al. Furthermore, auxin regulates the expression of BR biosynthesis genes, and hence, are linked directly with BR biosynthesis Chung et al.
In Arabidopsis , the exogenous treatment of auxin dramatically increased the transcript levels of DWF4 gene leading to enhancement in BR biosynthesis probably through induction of BRX protein Chung et al.
Furthermore, a close relationship between BR and auxin in plant growth and development has been established through interaction between BIN2 and auxin response factors ARF2.
It leads to the up-regulation of BR regulated genes and also promotes the activity of ARF promoters, enhancing auxin signaling, indicating BR-auxin synergistic interaction. Further studies indicate that in rice, auxin treatment enhances the transcript levels of BR receptor gene OsBRI1 suggesting that auxin regulates the level of BR receptors thus enhancing BR perception.
Recently, ChIP and yeast one-hybrid assay demonstrates a link between BR and auxin in controlling lamina inclination which is implicated in plant architecture development and grain yield Zhang et al. It has been observed that in OsGH3. Furthermore, an antagonistic interaction between BR and auxin has been linked through the transcription factor BZR1 in roots of Arabidopsis , to control the spatiotemporal balance of stem cell dynamics required for optimum root growth Chaiwanon and Wang, It has been observed that the optimum amount of BZR1 expression patterns required for root growth is established through local BR catabolism, auxin biosynthesis and BR signaling.
BZR1 activates the target genes expressed in the transition-elongation zone, but represses genes in the quiescent center and surrounding stem cells, however, on contrary, auxin has an opposite effect to BR on the spatiotemporal gene expression Chaiwanon and Wang, Recently, the actin cytoskeleton was reported to play an essential role in integrating BR and auxin responses.
Since, it has been demonstrated that BR alter cytoskeletal configuration in a manner similar to that of auxin. Moreover, BR-mediated reconfiguration of actin cytoskeleton causes delocalization of the PIN2 transporters, thus promoting auxin responses Lanza et al.
It indicates toward the possible role of BR and auxin crosstalk in abiotic stress tolerance through auxin transporter genes. Furthermore, rice genome acquires seven YUCCA genes which encode the rate limiting enzymes for auxin biosynthesis Yamamoto et al.
Although the relationship of BR and auxin has been well documented primarily in plant growth and developmental processes, however, further investigations are prerequisite to understand the mechanism of auxin and BR crosstalk involved in abiotic stress tolerance.