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The Control of Cell Expansion, Cell Division, and Vascular Development by Brassinosteroids: a Historical Perspective

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International Journal of Molecular Sciences Review The Control of Cell Expansion, Cell Division, and Vascular Development by Brassinosteroids: A Historical Perspective Man-Ho Oh 1 , Saxon H. Honey 2 and Frans E. Tax 2,* 1 Department of Biological Sciences, College of Biological Sciences and Biotechnology, Chungnam National University, Daejeon 34134, Korea; [email protected] 2 Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USA; [email protected] * Correspondence: [email protected] Received: 21 January 2020; Accepted: 22 February 2020; Published: 4 March 2020 Abstract: Steroid hormones are important signaling molecules in plants and animals. The plant steroid hormone brassinosteroids were first isolated and characterized in the 1970s and have been studied since then for their functions in plant growth. Treatment of plants or plant cells with brassinosteroids revealed they play important roles during diverse developmental processes, including control of cell expansion, cell division, and vascular differentiation. Molecular genetic studies, primarily in Arabidopsis thaliana, but increasingly in many other plants, have identified many genes involved in brassinosteroid biosynthesis and responses. Here we review the roles of brassinosteroids in cell expansion, cell division, and vascular differentiation, comparing the early physiological studies with more recent results of the analysis of mutants in brassinosteroid biosynthesis and signaling genes. A few representative examples of other molecular pathways that share developmental roles with brassinosteroids are described, including pathways that share functional overlap or response components with the brassinosteroid pathway. We conclude by briefly discussing the origin and conservation of brassinosteroid signaling. Keywords: brassinosteroids; cell expansion; cell elongation; cell division; vascular differentiation; Arabidopsis thaliana 1. Introduction Brassinosteroids (BRs) are an essential plant hormone and are now considered at the same level as the classic plant hormones auxin, cytokinin, ethylene, gibberellic acid, and abscisic acid. This is due to the important roles of BRs in regulating developmental processes also controlled by the classic plant hormones such as cell expansion, cell division, and differentiation, and because of the well-characterized biosynthesis and signaling pathways of BRs. In this review, we take a historical perspective and begin by describing the initial chemical characterization of plant steroid hormones and their bioactivity in different plant-based assays for cell elongation, cell division, and vascular development. Next, we describe the identification of the components of the signaling pathway that perceives BRs, which is one of the best-characterized pathways in plants. We discuss the genetic evidence for the roles of the BR pathway components in the developmental processes of cell elongation, in the control of cell division, and in vascular development. Other influences or pathways that participate in cell elongation are also discussed, including potential integration points with some signaling pathways of the classic plant hormones. Finally, we summarize the evidence for the conservation of BR signaling throughout the plant kingdom. Below is a timeline (Figure1) that delineates some of the key breakthroughs in BR research. Int. J. Mol. Sci. 2020, 21, 1743; doi:10.3390/ijms21051743 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, 1743 2 of 15 Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 15 Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 15 Figure 1.Figure Key breakthroughs 1. Key breakthroughs in the timeline in the timelineof research of research on brassinosteroids. on brassinosteroids [1–11] [1–11]. Figure 1. Key breakthroughs in the timeline of research on brassinosteroids. [1–11] 2.2. Brassinosteroids-StructureBrassinosteroids-Structure and and Functions Functions 2. Brassinosteroids-Structure and Functions 2.1.2.1. TheThe Isolation Isolation of of Brassinosteroids, Brassinosteroids, Plant Plant Steroid Steroid Hormones Hormones 2.1. The Isolation of Brassinosteroids, Plant Steroid Hormones TheThe discovery discovery of of brassins, brassins, a a naturally naturally occurring occurring group group of of plant-growth-promoting plant-growth-promoting substances substances purifiedpurifiedThe fromdiscoveryfrom pollen,pollen, of brassins, waswas firstfirst a naturally reportedreported occurring byby aa researchresearch group groupofgroup plant atat-growth thethe United United-promoting StatesStates substances DepartmentDepartment ofof AgriculturepurifiedAgricultur frome [ 1[1] ].pollen,.To To obtain obtain was first enough enough reported crude crude by extract, extract,a research about about group 225 225 kgat kg the of of bee-collected Unitedbee-collected States Brassica DepartmentBrassica napus napus ofpollen pollen wasAgriculturwas processed processede [1] via. To via aobtain pilot a pilot plant-sizeenough plant crude solvent-size extract, solvent extraction about extraction 225 procedure kg of procedure bee and-collected partially and Brassica purifiedpartially napus [12 purifiedpollen]. Following [12]. thiswasFollowing purification,processed this via purification, crystals a pilot were plant crystals obtained-size solvent were and subjectedextractionobtained toandprocedure X-ray subjected crystallography and partiallyto X-ray purified tocrystallography determine [12]. their to structureFollowingdetermine [ 2 this].their The purification, structure isolation andcrystals[2]. structuralThe were isolation obtained elucidation and and structural of subjected brassin elucidation [to2], X a- novelray crystallographyof polyhydroxysteroidal brassin [2] , toa novel determine their structure [2]. The isolation and structural elucidation of brassin [2], a novel lactonepolyhydroxysteroidal with strong plant lactone growth-promoting with strong plant activity, growth was-promoting the beginning activity, of was intensive the beginning study ofof polyhydroxysteroidal lactone with strong plant growth-promoting activity, was the beginning of aintensive new class study ofphytohormones, of a new class termedof phytoho brassinosteroidsrmones, termed (BRs). brassinosteroids The most biologically (BRs). The active most plant-growth-promotingintensive study of a new steroid class is of brassinolide phytohormones, (BL, C28H48O6, termed brassinosteroids MW = 480, see Figure(BRs).2 ).The The most structures biologicallybiologically active active plant plant-growth-growth-promoting-promoting steroid steroid is brassinolide is brassinolide (BL, C28H48O6,(BL, C28H48O6, MW = MW480, see= 480, see of BL, 24-Epibrassinolide (another naturally occurring BR), and progesterone, for comparison, are FigureFigure 2).2). TheThe structuresstructures of ofBL, BL, 24 -Epibrassinolide24-Epibrassinolide (another (another naturally naturally occurring occurring BR), andBR), and shown in Figure2. 24-Epibrassinolide was one of the first BRs to be synthesized e fficiently in the progesterone,progesterone, for for comp comparison,arison, are are shown shown in Figure in Figure 2. 24 2.-Epibrassinolide 24-Epibrassinolide was one was of one the firstof the BRs first to BRs to lab [13]. bebe synthesizedsynthesized efficiently efficiently in inthe the lab lab [13] [13]. FigureFigure 2.2. TheThe structurestructure ofof brassinolidebrassinolide andand 24-epibrassinolide,24-epibrassinolide, plantplant steroidsteroid hormoneshormones relatedrelated toto animal Figure 2. The structure of brassinolide and 24-epibrassinolide, plant steroid hormones related to steroidanimal steroid hormone hormone progesterone. progesteron Sidee. Side chains chains that that are are structurally structurally conserved conserved are indicated indicated in in red; red; side animal steroid hormone progesterone. Side chains that are structurally conserved are indicated in red; chainsside chains that that diff erdiffer between between the the hormones hormones are are in in black. black. side chains that differ between the hormones are in black. 2.2.2.2. Biological Activities Activities of of Brassinosteroids Brassinosteroids 2.2. Biological Activities of Brassinosteroids BrassinosteroidsBrassinosteroids were were initially initially characterized characterized for fortheir their growth growth-promoting-promoting effects eff inects plants. in plants. Plant Plant growthgrowthBrassinosteroids couldcould theoretically theoretically were be be initially stimulated stimulated characterized by by changes changes infor cellin their cell elongation growthelongation- (cellspromoting (cells expanding expanding effects in onein in plants. dimensionone Plant dimensiongrowth could to elongate theoretically cells and be organs) stimulated or expansion by changes (cells expandingin cell elongation in all three (cells dimensions), expanding by in one dimension to elongate cells and organs) or expansion (cells expanding in all three dimensions), by Int. J. Mol. Sci. 2020, 21, 1743 3 of 15 toInt. elongate J. Mol. Sci. cells2020, 2 and1, x FOR organs) PEER REVIEW or expansion (cells expanding in all three dimensions), by cell3 of division, 15 or by changes in differentiation. In this section, we will summarize the results of BR assays that measurecell division, cell expansion,or by changes cell in division, differentiati andon. vascular In this disection,fferentiation we will (as summarize an example the ofresults differentiation). of BR BRsassays are that also measure implicated cell in
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