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Research Progress on the Roles of Cytokinin in Plant Response to Stress

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Research Progress on the Roles of Cytokinin in Plant Response to Stress International Journal of Molecular Sciences Review Research Progress on the Roles of Cytokinin in Plant Response to Stress Yun Liu y, Mingjing Zhang y, Zhe Meng , Baoshan Wang * and Min Chen * Shandong Provincial Key Laboratory of Plant Stress Research, College of Life Science, Shandong Normal University, Jinan 250014, China; [email protected] (Y.L.); [email protected] (M.Z.); [email protected] (Z.M.) * Correspondence: [email protected] (B.W.); [email protected] or [email protected] (M.C.); Tel.: +86-531-86180745 (B.W. & M.C.); Fax: +86-531-86180107 (B.W. & M.C.) These authors contributed equally to this work. y Received: 16 August 2020; Accepted: 3 September 2020; Published: 8 September 2020 Abstract: Cytokinins promote plant growth and development under normal plant growth conditions and also play an important role in plant resistance to stress. Understanding the working mechanisms of cytokinins under adverse conditions will help to make full use of cytokinins in agriculture to increase production and efficiency of land use. In this article, we review the progress that has been made in cytokinin research in plant response to stress and propose its future application prospects. Keywords: abiotic stress; cytokinins; plant resistance; research progress 1. Introduction Cytokinins are one of the five major types of plant hormones that play an important role in the cell cycle and affect the growth and development of plants [1]. In addition to promoting cell division and plant growth and development, cytokinins also impede plant senescence by inhibiting the decomposition of chlorophyll, nucleic acids, proteins, and other substances in plants and redistributing necessary amino acids, hormones, inorganic salts, and other compounds to other parts of the plant [2]. An increasing amount of research shows that cytokinins can alleviate the damage to plants caused by a variety of abiotic stresses [3–5]. However, under adversity stress, mechanisms of cytokinin-alleviating stress are different under different stresses. Can the mechanism of cytokinin alleviating one stress be used for other stresses and can it be understood from the perspective of cross adaptation? In this review, cytokinin synthesis, metabolism, signaling pathways, and research progress on these topics in regards to plant resistance to stress (cold, heat, salt, and drought stress) and its future application prospects are discussed. 2. Synthesis and Metabolism Almost all organisms produce cytokinins (CKs). Natural cytokinins are adenine derivatives with isoprenoid or aromatic side chains at the N6 position of the adenine ring [6]. Therefore, natural cytokinins can be divided into isoprenoid and aromatic CKs, where the former is more commonly found in plants and more abundant than the latter [7]. Isoprenoid CKs are primarily composed of iP (isopentenyl adenine), tZ (trans-zeatin), cZ (cis-zeatin), and DZ (dihydrozeatin), of which iP and tZ are considered the main active cytokinins [7,8]. The aromatic cytokinins include orthotopolin (oT), mesotopolin (mT), their methoxy derivatives (MeoT and MemT, respectively), benzyladenine (BA), and others. These, however, are only found in some plant species such as poplar and tobacco [7,8]. In addition to natural cytokinins, there are also some synthetic cytokinins, such as kinetin, 6-benzylaminopurine (6-BA), Int. J. Mol. Sci. 2020, 21, 6574; doi:10.3390/ijms21186574 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, 6574 2 of 18 Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 17 benzylaminopurinebenzyladenine, and trans-zeatin(6-BA), benzyladenine, riboside that and exhibit trans-zeatin cytokinin riboside activity andthat canexhibit affect cytokinin plant growth activity via andan external can affect application. plant growth via an external application. Synthetic precursors ofof cytokinincytokinin and and its its synthesis synthesis process process rely rely on on the the terpenoid terpenoid pathway. pathway. The The key keyenzymes enzymes involved involved in cytokinin in cytokinin biosynthesis biosynthesis are isopentenyl are isopentenyl transferase transferase (IPT) and(IPT) LONELY and LONELY GUY (LOG) GUY (LOG)(Figure (Figure1)[ 9]. IPTs 1) [9]. are IPTs the centralare the rate-limiting central rate-limiting enzymes enzymes for cytokinin for cytokinin biosynthesis biosynthesis and are composed and are composedof adenosine of phosphate-isopentenyladenosine phosphate-isopentenyl transferases tr andansferases tRNA-isopentenyl and tRNA-isopentenyl transferases (tRNA-IPTs).transferases (tRNA-IPTs).The common featureThe common of these feature two types of ofthese IPTs two is a type conserveds of IPTs IPPT-binding is a conserved domain IPPT-binding [7]. The iP-ribotides domain [7].are precursorsThe iP-ribotides of iP [8are]. Theprecursors adenosine of iP phosphate-isopentenyl [8]. The adenosine phosphate-isopentenyl transferases can catalyze transferases dimethylallyl can catalyzediphosphate dimethylallyl (DMAPP) todiphosphate form iP-ribotides, (DMAPP) which initiatesto form cytokinin iP-ribotides, biosynthesis which [7initiates]. Then iP-ribotides cytokinin biosynthesisare catalyzed [7]. by cytochromeThen iP-ribotides P450 monooxygenase are catalyzed by CYP735As cytochrome into P450 tZ-ribotides monooxygenase [10] and thisCYP735As process into also tZ-ribotidesplays an important [10] and role this in process promoting also plays the growth an important of Arabidopsis role inshoots promoting [6]. These the growth iP- and of tZ-ribotides Arabidopsis shootsare the [6]. precursors These iP- ofand most tZ-ribotides iP-type andare the tZ-type precur cytokinins,sors of most which iP-type can and generate tZ-type iP cytokinins, and tZ through which canribosides generate [8]. iP The and biosynthesis tZ through ribosides of cZ is initiated[8]. The bi byosynthesis tRNA-IPTs, of cZ which is initiated use DMAPP by tRNA-IPTs, to catalyze which the useprenylation DMAPP ofto tRNAcatalyze and the then prenylation further generateof tRNA cZ-ribotidesand then further (Figure generate1)[ 7]. cZ-ribotides IPTs are encoded (Figure by1) [7].multiple IPTs geneare encoded families by in somemultiple plants gene [11 families], for example, in some 9 IPTsplants(AtIPT1-AtIPT9 [11], for example,) have 9 been IPTsidentified (AtIPT1- AtIPT9in Arabidopsis) have been[11], identified 10 IPTs (OsIPT1 in Arabidopsis-OsIPT10 [11],) in rice10 IPTs [12], (OsIPT1 and 7 FvIPTs-OsIPT10in the) in strawberryrice [12], and genome 7 FvIPTs [3]. inLOGs the strawberry are a new cytokinin-activating genome [3]. LOGs are enzyme a new with cyto akinin-activating conserved lysine enzyme decarboxylase-binding with a conserved domain lysine decarboxylase-bindingin all the proteins expressed domain by LOGsin all [the3]. Throughproteins expressed its cytokinin-specific by LOGs [3]. phosphohydrolase Through its cytokinin- activity, specificLOGs directly phosphohydrolase convert the inactiveactivity, cytokininLOGs directly ribotides convert into the a biologically inactive cytokinin active free ribotides base form into [ 8a]. biologicallyLOGs were firstactive discovered free base form in rice, [8]. and LOGs the were nine firstLOGs discovered(AtLOG1-AtLOG9 in rice, and) found the nine in Arabidopsis LOGs (AtLOG1-were AtLOG9later considered) found toin beArabidopsis the rice homologs were later [9 ].considered The strawberry to be genomethe rice recentlyhomologs identified [9]. The nine strawberryFvLOGs . genomeThe expression recently of identified most FvIPTs nineand FvLOGsFvLOGs. Thechanges expression under of osmotic most FvIPTs stress, and high FvLOGs temperature changes treatment, under osmoticand exogenous stress, high abscisic temperature acid (ABA), treatment, suggesting and thatexog theseenous genes abscisic may acid play (ABA), a role suggesting in plant resistance that these to genesabiotic may stresses play [a3 ].role in plant resistance to abiotic stresses [3]. FigureFigure 1. 1. SimplifiedSimplified model model of of cytokinin cytokinin biosynthesis biosynthesis and and decomposition decomposition pathways. The maintenance of cytokinin in plants requires fine control of the biosynthesis and metabolic The maintenance of cytokinin in plants requires fine control of the biosynthesis and metabolic enzymes. Therefore, the maintenance of stable cytokinin content requires not only cytokinin synthetase enzymes. Therefore, the maintenance of stable cytokinin content requires not only cytokinin but also cytokinin-metabolizing enzymes [13]. The level of active cytokinin can be regulated by binding synthetase but also cytokinin-metabolizing enzymes [13]. The level of active cytokinin can be to sugars (most commonly glucose) or by irreversible cleavage of cytokinin oxidases (CKXs) [14]. regulated by binding to sugars (most commonly glucose) or by irreversible cleavage of cytokinin The binding of glucose to cytokinin occurs at the N3,N7, and N9 positions of the purine ring or the oxidases (CKXs) [14]. The binding of glucose to cytokinin occurs at the N3, N7, and N9 positions of the hydroxyl group of the pentenyl side chain, including O and N-glycosylation [8]. O-glycosylation purine ring or the hydroxyl group of the pentenyl side chain, including O and N-glycosylation [8]. occurs on the oxygen of the cytokinin side chain, which is catalyzed by glucosyltransferase and O-glycosylation occurs on the oxygen of the cytokinin side chain, which is catalyzed by reversed by β-glucosidase [7]. N-glycosylation, which mainly occurs on the N7 or N9 of the purine glucosyltransferase
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