《植物生物学》课程教学资源（文献资料）Wang2020_Article_InitiationAndMaintenanceOfPlan

aBIOTECHhttps://doi.org/10.1007/s42994-020-00020-3aBIOTECHREVIEWCCupdateerInitiation and maintenance of plant stem cells in rootand shoot apical meristemsJunxia Wang', Yinghua Su?, Xiangpei Kong', Zhaojun DingiXian Sheng Zhang21The Key Laboratoryof PlantDevelopment and Environmental Adaptation Biology,Ministry ofEducation, CollegeofLifeSciences,ShandongUniversity,Qingdao266237,Shandong,China2 State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University.Tai'an 271018, Shandong, ChinaReceived:4March2020/Accepted:7April 2020AbstractPlant stem cells are a small group of cells with a self-renewal capacity and serve as a steady supply ofprecursor cellstoform new differentiated tissues and organs inplants.Root stem cells and shoot stemcells, which are located in the root apical meristem and in the shootapical meristem,respectively,playacritical role inplantlongitudinal growth.These stem cells inshoot and root apicalmeristems remainaspluripotent statethroughout the lifespanof theplantand control thegrowthand developmentofplants.The molecular mechanisms of initiation and maintenance of plant stem cells have beenextensivelyinvestigated.Inthisreview,wemainlydiscuss howtheplantphytohormones,suchas auxinand cytokinin,coordinate with thekeytranscription factors to regulate plant stem cell initiation andmaintenance in root and shoot apical meristems.In addition, we highlight the common regulatorymechanisms of both rootand shootapical meristems.Keywords Stem cell, Initiation, Maintenance, Auxin, Cytokinin, Transcription factorsINTRODUCTIONThe stem cells aremaintained in specialized microen-vironments called stem cell niches(SCN)in which cellsAs in animals,theplants possess small populations ofare maintained as stem cells, where the intra-and extra-stem cells,which arelocated in themeristems and arecellular signals are available and coordinated to main-defined by theability to renewthemselves and con-tain the stem cell identity (Jiang and Feldman 2005). Intribute undifferentiated daughter cells to produce newaddition, stem cells also reside in lateral meristemtissues (Heidstra and Sabatini 2014).The best charac-including cambiumand phellogen,and intercalaryterized stem cell in the plant reside in the root apicalmeristem,which allow plants to grow radially andmeristem (RAM)and the shoot apical meristem (SAM),especiallydeterminetheshapeofinternodes,respec-whichcalledapicalmeristem,areresponsibleforplanttively (Sato-lzawa et al. 2012; Smetana et al. 2019)longitudinal growth.These stem cells remain asHere,wemainlydiscussthe initiation and maintenancepluripotent state throughout the lifespan of the plant.ofplant stem cells in root and shoot apical meristems.The root stem cells are located in thetip of the root andinitiated during embryogenesis.While dividing,someJunxia Wang and Yinghua Su have contributed equally to thisdaughtercells remain stem stateand others contributework.to the cells of all the tissues in the root including root Correspondence: dingzhaojun@sdu.edu.cn (z. Ding),cap, epidermis, cortex, endodermis, and vascular tissueszhangxs@sdau.edu.cn (X.S.Zhang) Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020Published online: 04 May 2020

REVIEW Initiation and maintenance of plant stem cells in root and shoot apical meristems Junxia Wang1 , Yinghua Su2 , Xiangpei Kong1 , Zhaojun Ding1& , Xian Sheng Zhang2& 1 The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, College of Life Sciences, Shandong University, Qingdao 266237, Shandong, China 2 State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Tai’an 271018, Shandong, China Received: 4 March 2020 / Accepted: 7 April 2020 Abstract Plant stem cells are a small group of cells with a self-renewal capacity and serve as a steady supply of precursor cells to form new differentiated tissues and organs in plants. Root stem cells and shoot stem cells, which are located in the root apical meristem and in the shoot apical meristem, respectively, play a critical role in plant longitudinal growth. These stem cells in shoot and root apical meristems remain as pluripotent state throughout the lifespan of the plant and control the growth and development of plants. The molecular mechanisms of initiation and maintenance of plant stem cells have been extensively investigated. In this review, we mainly discuss how the plant phytohormones, such as auxin and cytokinin, coordinate with the key transcription factors to regulate plant stem cell initiation and maintenance in root and shoot apical meristems. In addition, we highlight the common regulatory mechanisms of both root and shoot apical meristems. Keywords Stem cell, Initiation, Maintenance, Auxin, Cytokinin, Transcription factors INTRODUCTION As in animals, the plants possess small populations of stem cells, which are located in the meristems and are defined by the ability to renew themselves and con￾tribute undifferentiated daughter cells to produce new tissues (Heidstra and Sabatini 2014). The best charac￾terized stem cell in the plant reside in the root apical meristem (RAM) and the shoot apical meristem (SAM), which called apical meristem, are responsible for plant longitudinal growth. These stem cells remain as pluripotent state throughout the lifespan of the plant. The stem cells are maintained in specialized microen￾vironments called stem cell niches (SCN) in which cells are maintained as stem cells, where the intra- and extra￾cellular signals are available and coordinated to main￾tain the stem cell identity (Jiang and Feldman 2005). In addition, stem cells also reside in lateral meristem including cambium and phellogen, and intercalary meristem, which allow plants to grow radially and especially determine the shape of internodes, respec￾tively (Sato-Izawa et al. 2012; Smetana et al. 2019). Here, we mainly discuss the initiation and maintenance of plant stem cells in root and shoot apical meristems. The root stem cells are located in the tip of the root and initiated during embryogenesis. While dividing, some daughter cells remain stem state and others contribute to the cells of all the tissues in the root including root cap, epidermis, cortex, endodermis, and vascular tissues Junxia Wang and Yinghua Su have contributed equally to this work. & Correspondence: dingzhaojun@sdu.edu.cn (Z. Ding), zhangxs@sdau.edu.cn (X. S. Zhang) Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020 aBIOTECH https://doi.org/10.1007/s42994-020-00020-3 aBIOTECH

aBIOTECH2002; Rademacher et al.2012).The auxin-dependentin the root elongationand differentiation zone (Perilliet al.2012).The shoot stem cells arelocated in the tip oftranscriptionfactorARF5/MPpromotesauxintransportthe shoot and share the similar developmental patternfromthe embryotothehypophysisprecursorthroughto root stem cells.When the shoot stem cellsdivide,positively regulating expression of the auxin efflux car-rierPIN-FORMED 1(PIN1),thereforeprovidingposi-somedaughtercellsremainstemcellstateinasmallrestrained region to keep self-renewal, while the othertionalsignalsfor roothypophysisspecificationdaughter cells will become incorporated into all the(Benkova et al. 2003; Friml et al. 2004; Weijers et al.2005,2006).aerial organs and tissues of the plant, such as shoot axis,The basic helix-loop-helix (bHLH) transcriptionalleaves,flowers,and side branches (Galliand Gallavotti2016;Zhang and Xue 2013).Thus,the initiation andregulatorTMo7,whichistranscriptionallycontrolled bymaintenanceof stem cells inroot and shoot apicalARF5/MP, acts downstream of ARF5-BDL auxin signal-meristems are essential for elaboration of plant body.ing module to control root stem cell initiation. In theearly embryos,thedecreaseof TMo7causes aberrantThemolecular mechanisms underlyingtheinitiationdivisions of the hypophysis and its descendants.TMo7and maintenance of plant stem cells have been exten-sively studied.Investigations on shootand root stemmovesfromthehypophysis-adjacentembryocellscells show that they share the common molecularwhere it is synthesized to the hypophysis, as suchmechanisms and also display distinctive characteristicscontributing to MP-dependent root apical meristemduring development.Coordination among complicatedformation (Schlereth et al. 2010).Another bHLH tran-signaling networks consists of theactivities of manykeyscriptional regulator TMO5,which is also targeted bytranscription factors and planthormones,whichgov-Mp, is expressed and functions in both the upper andernsthe establishment and organizationof boththelowerembryotomediatebothshootand rootstemcellRAM and SAM, and is required for maintaining theinitiation (Schlereth et al.2010).The homeodomainbalance of stem cells and determining cell identityinthe(PHD) finger proteins OBERON1 (OBE1), OBE2, TITA-NIA1 (TTA1), and TTA2 are reported to act in MP-de-dynamic structure of both meristems (Wolters andJurgens 2009).Inthisreview,wefocuson themolecularpendent root initiation.Double mutations in the closelymechanisms of stem cell initiation and maintenance inrelated OBE1and OBE2or inTTA1andTTA2genes leadto rootless defects that are very similar to thoserootand shootapicalmeristemsofArabidopsis,espe-observed in mp mutants (Saiga et al. 2008, 2012; Tho-cially the hormonal signaling interactions betweenmas et al. 2009). Furthermore, ARF5/MP can directlyauxin and cytokinin, and thecoordination of hormonesbind to NO TRANSMITTING TRACT (NTT) regulatorywithkeytranscriptionfactors.We also summarizetherecentknowledgeaboutthecommonmolecularmech-sequences to promote its expression in root-meristemanism of stem cell initiation and maintenance inbothinitiation.NTT, encoding a putative zinc-finger tran-RAMand SAM.scription factor and twocloselyrelated paralogs WIPDOMAIN PROTEIN 4 (WIP4) and WIP5 are required forthe initiation of the root meristem (Crawford et al.PLANT STEM CELLINITIATION2015).Insummary,ARF5/MP-BDLmodule-mediatedauxin signaling controls root stem cell initiation throughRoot stemcell initiationthe key transcription factors such as TM05/7, OBE1/2,TAA1/2, NTT, and so on (Fig. 1A).Stem cells resideinthe center of themeristem.BothShoot stem cell initiationroot and shoot apical meristems are initiated duringembryogenesis.Root apical meristem isinitiated fromThe shoot meristem becomes histologicallyvisibletheasymmetric division of theuppermost suspensorcell, orhypophysis,at the lateglobular stage.Thebasalduring mid-stage embryogenesis with the typical three-lens-shaped daughter,theprogenitor of the quiescentlayered structurebetween the cotyledons (Jurgens et al.center, gives rise to the distal root cap derived from1994).Expressionoftheshootmeristemstemcellasymmetric division (Jeong et al. 2011). In the initiationmarker CLAVATA3 (CLV3)becomes detectablein transi-of root apical meristem,auxin plays a critical role (Detion stage embryos.Thekey regulatorgene of stem cellSmet 2010; Dolan et al. 1993; Lau et al. 2008). Auxinhomeostasis WUSCHEL (WUS) is first expressed inregulates embryonic root stem cell initiation throughprogenitor cells of the organizing center (oC) thattheactionoftheAUXINRESPONSEFACTOR5(ARF5)/dynamically maintainsthe size of the stem cell pool inMONOPTEROS(MP)transcriptionfactorand itsauxin-the 16-cell stage embryo (Mayer et al.1998).It islabileinhibitorIAA12/BODENLOS(BDL)(Hamann etal.reported that wUs is expressed but dispensable for Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020

in the root elongation and differentiation zone (Perilli et al. 2012). The shoot stem cells are located in the tip of the shoot and share the similar developmental pattern to root stem cells. When the shoot stem cells divide, some daughter cells remain stem cell state in a small restrained region to keep self-renewal, while the other daughter cells will become incorporated into all the aerial organs and tissues of the plant, such as shoot axis, leaves, flowers, and side branches (Galli and Gallavotti 2016; Zhang and Xue 2013). Thus, the initiation and maintenance of stem cells in root and shoot apical meristems are essential for elaboration of plant body. The molecular mechanisms underlying the initiation and maintenance of plant stem cells have been exten￾sively studied. Investigations on shoot and root stem cells show that they share the common molecular mechanisms and also display distinctive characteristics during development. Coordination among complicated signaling networks consists of the activities of many key transcription factors and plant hormones, which gov￾erns the establishment and organization of both the RAM and SAM, and is required for maintaining the balance of stem cells and determining cell identity in the dynamic structure of both meristems (Wolters and Jurgens 2009). In this review, we focus on the molecular mechanisms of stem cell initiation and maintenance in root and shoot apical meristems of Arabidopsis, espe￾cially the hormonal signaling interactions between auxin and cytokinin, and the coordination of hormones with key transcription factors. We also summarize the recent knowledge about the common molecular mech￾anism of stem cell initiation and maintenance in both RAM and SAM. PLANT STEM CELL INITIATION Root stem cell initiation Stem cells reside in the center of the meristem. Both root and shoot apical meristems are initiated during embryogenesis. Root apical meristem is initiated from the asymmetric division of the uppermost suspensor cell, or hypophysis, at the late globular stage. The basal lens-shaped daughter, the progenitor of the quiescent center, gives rise to the distal root cap derived from asymmetric division (Jeong et al. 2011). In the initiation of root apical meristem, auxin plays a critical role (De Smet 2010; Dolan et al. 1993; Lau et al. 2008). Auxin regulates embryonic root stem cell initiation through the action of the AUXIN RESPONSE FACTOR 5 (ARF5)/ MONOPTEROS (MP) transcription factor and its auxin￾labile inhibitor IAA12/BODENLOS (BDL) (Hamann et al. 2002; Rademacher et al. 2012). The auxin-dependent transcription factor ARF5/MP promotes auxin transport from the embryo to the hypophysis precursor through positively regulating expression of the auxin efflux car￾rier PIN-FORMED 1 (PIN1), therefore providing posi￾tional signals for root hypophysis specification (Benkova et al. 2003; Friml et al. 2004; Weijers et al. 2005, 2006). The basic helix–loop–helix (bHLH) transcriptional regulator TMO7, which is transcriptionally controlled by ARF5/MP, acts downstream of ARF5-BDL auxin signal￾ing module to control root stem cell initiation. In the early embryos, the decrease of TMO7 causes aberrant divisions of the hypophysis and its descendants. TMO7 moves from the hypophysis-adjacent embryo cells where it is synthesized to the hypophysis, as such contributing to MP-dependent root apical meristem formation (Schlereth et al. 2010). Another bHLH tran￾scriptional regulator TMO5, which is also targeted by MP, is expressed and functions in both the upper and lower embryo to mediate both shoot and root stem cell initiation (Schlereth et al. 2010). The homeodomain (PHD) finger proteins OBERON1 (OBE1), OBE2, TITA￾NIA1 (TTA1), and TTA2 are reported to act in MP-de￾pendent root initiation. Double mutations in the closely related OBE1 and OBE2 or in TTA1 and TTA2 genes lead to rootless defects that are very similar to those observed in mp mutants (Saiga et al. 2008, 2012; Tho￾mas et al. 2009). Furthermore, ARF5/MP can directly bind to NO TRANSMITTING TRACT (NTT) regulatory sequences to promote its expression in root-meristem initiation. NTT, encoding a putative zinc-finger tran￾scription factor and two closely related paralogs WIP DOMAIN PROTEIN 4 (WIP4) and WIP5 are required for the initiation of the root meristem (Crawford et al. 2015). In summary, ARF5/MP-BDL module-mediated auxin signaling controls root stem cell initiation through the key transcription factors such as TMO5/7, OBE1/2, TAA1/2, NTT, and so on (Fig. 1A). Shoot stem cell initiation The shoot meristem becomes histologically visible during mid-stage embryogenesis with the typical three￾layered structure between the cotyledons (Jurgens et al. 1994). Expression of the shoot meristem stem cell marker CLAVATA3 (CLV3) becomes detectable in transi￾tion stage embryos. The key regulator gene of stem cell homeostasis WUSCHEL (WUS) is first expressed in progenitor cells of the organizing center (OC) that dynamically maintains the size of the stem cell pool in the 16-cell stage embryo (Mayer et al. 1998). It is reported that WUS is expressed but dispensable for Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020 aBIOTECH

aBIOTECHABAuxinYNOXYIAA12ARR7/15OBE1/2MPApillARFTTA1/21-TMO7TM05NTTCKsignaling-BDcellinitiatloStem cell initiationLens-shapedcelBasal-daughtercelCDCKCZLPAuxinPZPZY一小一一一日Quiescent centerVasculatureMEndodermisCortexEpidermisCDFCZ,centralzoneCYCDCortex/endodermis initialsPZ,peripheral zoneCLV40Distal stem cellLP, ateral primordiumDifferentiatedcolumellacellsizingcenteFig.1 Initiation and maintenance of plant stem cells in root and shoot apical meristems.A Initiation of root stem cells duringembryogenesis.Gene regulation in the initiation of stem cells in embryonic root apical meristem at thelateglobular stage.Antagonismbetween auxin and cytokinin determines the establishment of root stem cell niche. Auxin antagonizes cytokinin output by directtranscriptional activation of ARR7 and ARR15, feedback repressors of cytokinin signaling (CK signaling). Auxin regulates embryonic rootstem cell initiation through the action of the MP transcription factor and auxin-labile inhibitor IAA12. And auxin cooperates with sometranscription factors OBE1/2, TAA1/2, TMO5/7, and NTT to regulate the initiation of root stem cells. B Initiation of shoot stem cells duringembryogenesis. Gene regulation in the initiation of stem cells in embryonic shoot apical meristem at globular embryo stage. WOx2 isinvolved in the initiation of shoot stem cells through regulatingPIN1-dependent auxin transport.WOx2upregulatesthe HD-ziP Iltranscription factors, which seem to mediate WOx2 function in the initiation of shoot stem cell through regulating cytokinin biosynthesis.Thus, WOx2 and its redundant WOx paralogs are required for the initiation of the shoot stem cell by establishing a regulatory frameworkthat balances the cytokinin and auxin pathways. ZLL and TPL mediate the initiation of stem cells in the embryonic SAM which involves thenegative regulation of auxin signaling. C Regulatory pathways control the maintenance of root stem cells. Gene regulation in themaintenance of stem cells in root apical meristem. The QC-specific transcriptional regulation of WOx5 is directly restricted by ROW1, andalso regulated by CLE40-ACR4 regulatory module. WOX5 inhibits CYCD1;1, CYCD3;3, and CDF4 activity to control root stem cells.Andauxin induces the expression of TPST and RGF genes, and TPST in turn sulfates the RGF peptides to induce the expression of PLT.Coordination among cytokinin and auxin maintains the size of root meristem and ensures root growth. The two hormones through asimple regulatory circuit converging on the SHY2 protein, which is activated by cytokinin and inhibited by auxin and a repressor of auxinsignaling that negatively regulates the PIN. D Regulatory pathways control the maintenance of shoot stem cells. The central regulatorypathway for the maintenance of shoot stem cells includes an autoregulatory negative-feedback loop comprising stem cell-promotingtranscription factor WUS and differentiation-promoting peptide CLV3.Cytokinin positively regulates the maintenanceof shoot stem cellactivity.Afeedback module between wUS and cytokinin signaling pathway produces accurate positioning of stem cell niche.The spatialauxin-cytokinincrosstalkfortheshootstem cellmaintenancewasdeterminedbythenegativeregulation of theexpressionofIPT5andARR7/15 via the auxin signaling component ARFs, and in turn by the inhibition of YUCs expression via cytokinin-responsivefactorsstemcellinitiation duringembryogenesis.However,theinvolvinginrootstemcell initiation,auxinalsocontrolsWUshomologousgenessuchasWox2werefoundtobeshoot stemcell initiation during embryogenesis.involved in the initiation of shoot stem cells throughTOPLESS(TPL)encodesamemberoftheGroucho/PIN1-dependent auxin transport duringTup1-typetranscriptional corepressors and its mutantregulatingembryogenesis (Zhang et al.2017).Therefore, besidestopless-1(tpl-1)showedthe shootstobetransformedAgricultural Information Institute, ChineseAcademyof Agricultural Sciences 2020

stem cell initiation during embryogenesis. However, the WUS homologous genes such as WOX2 were found to be involved in the initiation of shoot stem cells through regulating PIN1-dependent auxin transport during embryogenesis (Zhang et al. 2017). Therefore, besides involving in root stem cell initiation, auxin also controls shoot stem cell initiation during embryogenesis. TOPLESS (TPL) encodes a member of the Groucho/ Tup1-type transcriptional corepressors and its mutant topless-1 (tpl-1) showed the shoots to be transformed Fig. 1 Initiation and maintenance of plant stem cells in root and shoot apical meristems. A Initiation of root stem cells during embryogenesis. Gene regulation in the initiation of stem cells in embryonic root apical meristem at the late globular stage. Antagonism between auxin and cytokinin determines the establishment of root stem cell niche. Auxin antagonizes cytokinin output by direct transcriptional activation of ARR7 and ARR15, feedback repressors of cytokinin signaling (CK signaling). Auxin regulates embryonic root stem cell initiation through the action of the MP transcription factor and auxin-labile inhibitor IAA12. And auxin cooperates with some transcription factors OBE1/2, TAA1/2, TMO5/7, and NTT to regulate the initiation of root stem cells. B Initiation of shoot stem cells during embryogenesis. Gene regulation in the initiation of stem cells in embryonic shoot apical meristem at globular embryo stage. WOX2 is involved in the initiation of shoot stem cells through regulating PIN1-dependent auxin transport. WOX2 upregulates the HD-ZIP III transcription factors, which seem to mediate WOX2 function in the initiation of shoot stem cell through regulating cytokinin biosynthesis. Thus, WOX2 and its redundant WOX paralogs are required for the initiation of the shoot stem cell by establishing a regulatory framework that balances the cytokinin and auxin pathways. ZLL and TPL mediate the initiation of stem cells in the embryonic SAM which involves the negative regulation of auxin signaling. C Regulatory pathways control the maintenance of root stem cells. Gene regulation in the maintenance of stem cells in root apical meristem. The QC-specific transcriptional regulation of WOX5 is directly restricted by ROW1, and also regulated by CLE40-ACR4 regulatory module. WOX5 inhibits CYCD1;1, CYCD3;3, and CDF4 activity to control root stem cells. And auxin induces the expression of TPST and RGF genes, and TPST in turn sulfates the RGF peptides to induce the expression of PLT. Coordination among cytokinin and auxin maintains the size of root meristem and ensures root growth. The two hormones through a simple regulatory circuit converging on the SHY2 protein, which is activated by cytokinin and inhibited by auxin and a repressor of auxin signaling that negatively regulates the PIN. D Regulatory pathways control the maintenance of shoot stem cells. The central regulatory pathway for the maintenance of shoot stem cells includes an autoregulatory negative-feedback loop comprising stem cell-promoting transcription factor WUS and differentiation-promoting peptide CLV3. Cytokinin positively regulates the maintenance of shoot stem cell activity. A feedback module between WUS and cytokinin signaling pathway produces accurate positioning of stem cell niche. The spatial auxin–cytokinin cross talk for the shoot stem cell maintenance was determined by the negative regulation of the expression of IPT5 and ARR7/15 via the auxin signaling component ARFs, and in turn by the inhibition of YUCs expression via cytokinin-responsive factors Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020 aBIOTECH

aBIOTECHinto roots at the apical role (Long et al. 2002, 2006),regulatoryframeworkthatbalancesthecytokininandindicating a crucial role of TPL during embryonic shootauxin pathways.stem cell initiation.TPL can physically interact withauxin repressor IAA12/BDL through an ETHYLENEAuxin interacts with cytokinin to control rootRESPONSEFACTOR(ERF)-aSSOciatedamphiphilicor shoot stem cell initiationrepression (EAR)motif,which thus mediates auxin-de-pendenttranscriptional repression and shootstem cellCytokinin is expressed in the suspensor of globularinitiation during embryogenesis (Szemenyei et al.embryos, which include the structure such as hypoph-2008).MutationofZWILLE(ZLL)leadstoanabsenceofysis,and plays an antagonistic role with auxin in themeristem in shoot apex, or with a differentiated leafrootapicalmeristeminitiation.Cytokininlevels(Moussianet al.1998).ZLL expression is first detecteddecreased in basal daughter cells, once the hypophysisthroughout the pro-embryo between the 2-cell andhas been divided. Nonetheless, the suspensor as well as8-cell stages and subsequently became restricted to thethe lens-shaped daughter cell kept high levels of cyto-vascular primordium, but are barely detectable in thekinin. On the contrary,the expression of auxin is only inshoot meristem until the embryo reaches maturitythe base of thehypophysis,but graduallydisappears in(Lynn et al. 1999; Moussian et al.1998; Tucker et al.lens-shapedcellsJeong et al.2011).Cytokinin2008).AuxinaccumulationandresponsesareenhancedresponsivefactorsARABIDOPSISRESPONSEREGULATORin zl embryos, and the transcription of ARF2 is upreg-(ARR)7andARR15are transcriptionally stimulatedbyulated.Downregulation of ARF2 in zll mutantscan sig-auxin during rootapical meristem initiation (Mullerandnificantlyrescuestemcell maintenance.Therefore,ZLL-Sheen 2008).mediated initiation of stem cells in the embryonic SAMDuringtheestablishmentof theembryonic shootorinvolves the negative regulation of auxin signalingrootmeristemin somaticembryogenesis of Arabidopsis,(Roodbarkelari et al. 2015)the early expression of theWUS and WUSCHEL-RELA-TEDHOMEOBOX5(WOx5)geneswasinduced,whichisCytokinin is also playing a crucial role in shoot stemcell initiation through the induction of SHOOTMER-essential for SAMand RAMinitiation andembryonicISTEMLESS(STM),which is involved inthespecificationshoot-root axis establishment (Su et al.2014).Cytoki-ofthecenterregionasembryonicSAMattheglobularnin and auxin signaling are correlated with inducedembryo stage through the interplay with CUP-SHAPEDWUS and WOx5 expression and subsequent embryonicCOTYLEDON (CUC) (Hibara et al. 2006;Takada et al.SAM and RAMformation during somaticembryogenesis2001).On onehand, CUC1and CUC2are involved in the(Su et al.2014).It was found thatARR7and ARR15inductionof STM expression (Aidaetal.1999).Ontheintegrate cytokinin and auxin signals and connect theseother hand,STM indirectlyrepresses theexpressionofinputs with the core regulatory machinery to initiateCUC1 and CUC2 genes by activating MIR164a, whichshoot apical meristem, but auxin plays a negative roletargets CUCmRNA,suggesting the potential for negativewhich is mediated through ARF5/MP transcription fac-feedbackloopsbetweenSTMandCUCgenes(Spinellitor (Zhao et al. 2010)etal.2011).STMalso setupapositivefeedbackloopthrough the regulation of cytokinin signaling in SAM(Jasinski et al.2005; Takada et al.2001;Yanai et al.PLANT STEM CELLMAINTENANCE2005). Thus, the interconnected STM-CUc negativefeedback loop together with the STM-cytokinin positiveRootstemcellmaintenancefeedback loop determines shoot stem cell initiation(Fig.1B).During embryonic shootstem cell formation,Duringthepost-embryonicgrowth,theplantsneedtoWOx2 upregulates the HD-ZIP III transcription factors,maintainthestem cell identity in root andshootwhich involves shoot apex fate and also regulates themeristemtokeepaplant'sindeterminategrowthwhichexpression of cytokinin biosynthetic geneIPT1inrootis essential for plant growth and development (Yang(Dello loio et al.2012).Expression of IPT1 is down-et al. 2019; Yao et al. 2019; Yu et al. 2019b, c).Theregulated in wox1235 mutants.Thus, HD-ZIPIII tran-primaryroot apical meristems arepopulationsof cellsscriptionfactors seemtomediateWox2function intheat the primary root tip that divide and form all the tis-initiation of shoot stem cell through regulatingcytokininsues of the root.The continuous growing of the primarybiosynthesis (Fig.1B).Itis shown thatWOX2,togetherroot in Arabidopsis islargelyresulted fromthesyner-with its redundant WOX paralogs, are required for thegetic process of cell division,elongation, and differen-initiation of the shoot stem cell by establishing atiation in theprimaryroot meristem (Benfeyetal.1993;Jiang and Feldman 2005; Lofke et al.2013;Zhao et al. Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020

into roots at the apical role (Long et al. 2002, 2006), indicating a crucial role of TPL during embryonic shoot stem cell initiation. TPL can physically interact with auxin repressor IAA12/BDL through an ETHYLENE RESPONSE FACTOR (ERF)-associated amphiphilic repression (EAR) motif, which thus mediates auxin-de￾pendent transcriptional repression and shoot stem cell initiation during embryogenesis (Szemenyei et al. 2008). Mutation of ZWILLE (ZLL) leads to an absence of meristem in shoot apex, or with a differentiated leaf (Moussian et al. 1998). ZLL expression is first detected throughout the pro-embryo between the 2-cell and 8-cell stages and subsequently became restricted to the vascular primordium, but are barely detectable in the shoot meristem until the embryo reaches maturity (Lynn et al. 1999; Moussian et al. 1998; Tucker et al. 2008). Auxin accumulation and responses are enhanced in zll embryos, and the transcription of ARF2 is upreg￾ulated. Downregulation of ARF2 in zll mutants can sig￾nificantly rescue stem cell maintenance. Therefore, ZLL￾mediated initiation of stem cells in the embryonic SAM involves the negative regulation of auxin signaling (Roodbarkelari et al. 2015). Cytokinin is also playing a crucial role in shoot stem cell initiation through the induction of SHOOTMER￾ISTEMLESS (STM), which is involved in the specification of the center region as embryonic SAM at the globular embryo stage through the interplay with CUP-SHAPED COTYLEDON (CUC) (Hibara et al. 2006; Takada et al. 2001). On one hand, CUC1 and CUC2 are involved in the induction of STM expression (Aida et al. 1999). On the other hand, STM indirectly represses the expression of CUC1 and CUC2 genes by activating MIR164a, which targets CUC mRNA, suggesting the potential for negative feedback loops between STM and CUC genes (Spinelli et al. 2011). STM also set up a positive feedback loop through the regulation of cytokinin signaling in SAM (Jasinski et al. 2005; Takada et al. 2001; Yanai et al. 2005). Thus, the interconnected STM-CUC negative feedback loop together with the STM-cytokinin positive feedback loop determines shoot stem cell initiation (Fig. 1B). During embryonic shoot stem cell formation, WOX2 upregulates the HD-ZIP III transcription factors, which involves shoot apex fate and also regulates the expression of cytokinin biosynthetic gene IPT1 in root (Dello Ioio et al. 2012). Expression of IPT1 is down￾regulated in wox1235 mutants. Thus, HD-ZIP III tran￾scription factors seem to mediate WOX2 function in the initiation of shoot stem cell through regulating cytokinin biosynthesis (Fig. 1B). It is shown that WOX2, together with its redundant WOX paralogs, are required for the initiation of the shoot stem cell by establishing a regulatory framework that balances the cytokinin and auxin pathways. Auxin interacts with cytokinin to control root or shoot stem cell initiation Cytokinin is expressed in the suspensor of globular embryos, which include the structure such as hypoph￾ysis, and plays an antagonistic role with auxin in the root apical meristem initiation. Cytokinin levels decreased in basal daughter cells, once the hypophysis has been divided. Nonetheless, the suspensor as well as the lens-shaped daughter cell kept high levels of cyto￾kinin. On the contrary, the expression of auxin is only in the base of the hypophysis, but gradually disappears in lens-shaped cells (Jeong et al. 2011). Cytokinin responsive factors ARABIDOPSIS RESPONSE REGULATOR (ARR) 7 and ARR15 are transcriptionally stimulated by auxin during root apical meristem initiation (Muller and Sheen 2008). During the establishment of the embryonic shoot or root meristem in somatic embryogenesis of Arabidopsis, the early expression of the WUS and WUSCHEL-RELA￾TED HOMEOBOX5 (WOX5) genes was induced, which is essential for SAM and RAM initiation and embryonic shoot–root axis establishment (Su et al. 2014). Cytoki￾nin and auxin signaling are correlated with induced WUS and WOX5 expression and subsequent embryonic SAM and RAM formation during somatic embryogenesis (Su et al. 2014). It was found that ARR7 and ARR15 integrate cytokinin and auxin signals and connect these inputs with the core regulatory machinery to initiate shoot apical meristem, but auxin plays a negative role which is mediated through ARF5/MP transcription fac￾tor (Zhao et al. 2010). PLANT STEM CELL MAINTENANCE Root stem cell maintenance During the post-embryonic growth, the plants need to maintain the stem cell identity in root and shoot meristem to keep a plant’s indeterminate growth which is essential for plant growth and development (Yang et al. 2019; Yao et al. 2019; Yu et al. 2019b, c). The primary root apical meristems are populations of cells at the primary root tip that divide and form all the tis￾sues of the root. The continuous growing of the primary root in Arabidopsis is largely resulted from the syner￾getic process of cell division, elongation, and differen￾tiation in the primary root meristem (Benfey et al. 1993; Jiang and Feldman 2005; Lofke et al. 2013; Zhao et al. Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020 aBIOTECH

aBIOTECH2014).In the root apex, there is a small group of cellstyrosine-sulfated peptides are linking auxin signaling towhich are rarely divided, called the quiescent centerPLT protein levels and controlling root stem cell identity(QC) (Dinneny and Benfey 2008; Jiang and Feldman(Matsuzaki etal.2010;Zhou etal.2010).Cytokinin signaling mediates cell differentiation at the2005).TheQC is crucial for maintaining the identities ofthe surrounding stem cells which havethe highest rateroottransition zonein Arabidopsis byrepressing bothof cell divisions.The WOx5 gene is specifically expres-auxin signaling and transport (Dello loio et al.2007)sedandfunctions inQCtoregulatethebalancebetweenCytokinin via the ARR1 control auxin distribution withincell division and differentiation of the adjacent stemthe meristem, generating an instructive auxin minimumcells (Sarkar et al.2007).that positionstheroot transition zone and guides rootAn auxin maximum is essential for themaintenancestem cell differentiation (Di Mambro et al.2017).Cyto-ofroot stemcell identityandguidesroot growthkinin was also found to act in the lateral root cap (LRC) to(Grieneisen et al. 2007; Moubayidin et al. 2013; Tiancoordinate cell differentiation of the root meristemet al.2014).Besides auxin efflux facilitators (PINs)-de-through the regulation of PIN5-mediated auxin intracel-pendent polar auxin transport (Grieneisen et al.2007),lulartransporterorviaIAA-amino synthase GRETCHENWOx5alsocoordinateslocal auxinproductionintheQCHAGEN3.17(GH3.17)mediatedauxinhomeostasis(Dioftheroot (Tianetal.2014).Furthermore,SCARECROWMambro et al.2019).The coordinated effect of thesetwo(SCR)isrequiredforthemaintenanceof rootmeristemhormones isessentialto maintain the sizeof rootthrough regulating the nuclear localization of SHORT-meristem and ensure rootgrowth.Moreover, cytokininRO0T (SHR) (Sabatini et al. 2003), and also involved inand auxin through a simple regulatory circuit convergesustaining root-associated auxin maximum through theon the SHY2 protein,a repressor of auxin signaling thatregulation of ARR1-ASB1 module-dependent auxinnegatively regulates the PIN. Specifically, SHY2 is acti-production (Moubayidin et al.2013).On theother hand,vated by either ARR1 or ARR12 and inhibited by auxinthis root-associated auxin maximum feeds back on(Delloloio etal.2008;Moubayidin etal.2010)WOX5 expression via IAA17-dependent regulation ofauxinresponses(DingandFriml2010;Tianetal.2014)ShootstemcellmaintenanceA feedback circuit betweenWOx5 activity and auxinsignaling maximum acts on theauxin-mediated rootInthemaintenanceof shootstemcells,theWUSproteinstemcell differentiation.However,auxin-repressedmigrates from the OC into superficial cell layers of theWOx5 expression might require a local signal in root QC,CZ to activate CLV3 transcription by binding to thesinceectopicallyexpressedWox5inrow1,defectedinaregulatoryregions of the CLV3promoter (Daum et al.repressor of wuschel1 (ROW1)which directlybindsto2014;Liuetal.2013;Peralesetal.2016).WUStheWox5 promoter region and restricts its transcrip-expression, in turn, is restricted in OC cells by a CLV3-tion, could not be repressed by auxin (Zhang et al.mediated signalingpathway(Brand etal.2000;Schoof2015).Besides auxin, CLAVATA3/ESR-RELATED40et al.2000; Song et al.2010; Willmann 2000).Thisregulates WOx5 expression throughthereceptor kina-WUS-CLVfeedbackloopinteractswiththedownstreamsesCRINKLY4(ACR4)(Stahletal.2009).WOX5main-response regulator of cytokinin signaling regulators,tains root stem cell niche identity through repression ofsuch as B-type and A-type ARR transcription factors tothe differentiation factorCDF4 or the inhibition oflimit SAM size(Dai et al.2017;Gordon et al.2009;CYCD1;1 and CYCD3;3 activity (Forzani et al. 2014; PiHwang et al. 2012). wUs directly suppresses severalet al.2015).negative A-type regulators (ARR5,ARR6,ARR7,andBesidesWOx5.AP2familytranscriptionfactorsPLEARR15) of cytokinin signaling (Leibfried et al. 2005),THORA (PLT)1,2,3and BABYBOOM (BBM)also outputthus enhancing downstream cytokinin responses in theauxin signalstodefinethe root stem cell niche in adosageSAM.Conversely,overexpression ofARR7 reduces WUSdependent manner (Aida et al.2004; Galinha et al.2007;expression,resulting inarrested shoot stem cell activityWang et al.2015).Thesymplastic signalingdirected localWhereas,downregulation of ARR7and ARR15 expres-auxinmaximadrivestheestablishmentofPLTgradientandsion inhibits CLV3 expression, indicating that CLV3root stem cell niche identity(Liu et al.2017).The recentexpression requires A-type ARRs but independent ofWUS activation (Zhao et al. 2010). Type-B ARRsreport alsoindicates thatauxin induces theexpression ofincludingARR1,ARR10,andARR12directlyactivatethetyrosylprotein sulfotransferase (TPST) and several theexpression of WUS (Fig.1D). Moreover, these ARRsROOTGROWTHFACTOR(RGF)genes.TPSTinturnsulfatestheRGFpeptides,which,byan unknown mechanism,directly repress the expression of YUCs,and indirectlyinducetranscriptional and posttranscriptional upregula-promote WUS induction (Meng et al. 2017).Therefore,the feedback between wUs and cytokinin signalingtion ofthe PLTproteinlevels (Fig.1C).Thus, TPSTandRGF Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020

2014). In the root apex, there is a small group of cells which are rarely divided, called the quiescent center (QC) (Dinneny and Benfey 2008; Jiang and Feldman 2005). The QC is crucial for maintaining the identities of the surrounding stem cells which have the highest rate of cell divisions. The WOX5 gene is specifically expres￾sed and functions in QC to regulate the balance between cell division and differentiation of the adjacent stem cells (Sarkar et al. 2007). An auxin maximum is essential for the maintenance of root stem cell identity and guides root growth (Grieneisen et al. 2007; Moubayidin et al. 2013; Tian et al. 2014). Besides auxin efflux facilitators (PINs)-de￾pendent polar auxin transport (Grieneisen et al. 2007), WOX5 also coordinates local auxin production in the QC of the root (Tian et al. 2014). Furthermore, SCARECROW (SCR) is required for the maintenance of root meristem through regulating the nuclear localization of SHORT￾ROOT (SHR) (Sabatini et al. 2003), and also involved in sustaining root-associated auxin maximum through the regulation of ARR1-ASB1 module-dependent auxin production (Moubayidin et al. 2013). On the other hand, this root-associated auxin maximum feeds back on WOX5 expression via IAA17-dependent regulation of auxin responses (Ding and Friml 2010; Tian et al. 2014). A feedback circuit between WOX5 activity and auxin signaling maximum acts on the auxin-mediated root stem cell differentiation. However, auxin-repressed WOX5 expression might require a local signal in root QC, since ectopically expressed WOX5 in row1, defected in a repressor of wuschel1 (ROW1) which directly binds to the WOX5 promoter region and restricts its transcrip￾tion, could not be repressed by auxin (Zhang et al. 2015). Besides auxin, CLAVATA3/ESR-RELATED 40 regulates WOX5 expression through the receptor kina￾ses CRINKLY4 (ACR4) (Stahl et al. 2009). WOX5 main￾tains root stem cell niche identity through repression of the differentiation factor CDF4 or the inhibition of CYCD1;1 and CYCD3;3 activity (Forzani et al. 2014; Pi et al. 2015). Besides WOX5, AP2 family transcription factors PLE￾THORA (PLT) 1, 2, 3 and BABY BOOM (BBM) also output auxin signals to define the root stem cell niche in a dosage￾dependent manner (Aida et al. 2004; Galinha et al. 2007; Wang et al. 2015). The symplastic signaling directed local auxin maxima drives the establishment of PLTgradient and root stem cell niche identity (Liu et al. 2017). The recent report also indicates that auxin induces the expression of tyrosylprotein sulfotransferase (TPST) and several the ROOT GROWTH FACTOR (RGF) genes. TPST in turn sulfates the RGF peptides, which, by an unknown mechanism, induce transcriptional and posttranscriptional upregula￾tion of the PLT protein levels (Fig. 1C). Thus, TPSTand RGF tyrosine-sulfated peptides are linking auxin signaling to PLT protein levels and controlling root stem cell identity (Matsuzaki et al. 2010; Zhou et al. 2010). Cytokinin signaling mediates cell differentiation at the root transition zone in Arabidopsis by repressing both auxin signaling and transport (Dello Ioio et al. 2007). Cytokinin via the ARR1 control auxin distribution within the meristem, generating an instructive auxin minimum that positions the root transition zone and guides root stem cell differentiation (Di Mambro et al. 2017). Cyto￾kinin was also found to act in the lateral root cap (LRC) to coordinate cell differentiation of the root meristem through the regulation of PIN5-mediated auxin intracel￾lular transporter or via IAA-amino synthase GRETCHEN HAGEN 3.17 (GH3.17) mediated auxin homeostasis (Di Mambro et al. 2019). The coordinated effect of these two hormones is essential to maintain the size of root meristem and ensure root growth. Moreover, cytokinin and auxin through a simple regulatory circuit converge on the SHY2 protein, a repressor of auxin signaling that negatively regulates the PIN. Specifically, SHY2 is acti￾vated by either ARR1 or ARR12 and inhibited by auxin (Dello Ioio et al. 2008; Moubayidin et al. 2010). Shoot stem cell maintenance In the maintenance of shoot stem cells, the WUS protein migrates from the OC into superficial cell layers of the CZ to activate CLV3 transcription by binding to the regulatory regions of the CLV3 promoter (Daum et al. 2014; Liu et al. 2013; Perales et al. 2016). WUS expression, in turn, is restricted in OC cells by a CLV3- mediated signaling pathway (Brand et al. 2000; Schoof et al. 2000; Song et al. 2010; Willmann 2000). This WUS-CLV feedback loop interacts with the downstream response regulator of cytokinin signaling regulators, such as B-type and A-type ARR transcription factors to limit SAM size (Dai et al. 2017; Gordon et al. 2009; Hwang et al. 2012). WUS directly suppresses several negative A-type regulators (ARR5, ARR6, ARR7, and ARR15) of cytokinin signaling (Leibfried et al. 2005), thus enhancing downstream cytokinin responses in the SAM. Conversely, overexpression of ARR7 reduces WUS expression, resulting in arrested shoot stem cell activity. Whereas, downregulation of ARR7 and ARR15 expres￾sion inhibits CLV3 expression, indicating that CLV3 expression requires A-type ARRs but independent of WUS activation (Zhao et al. 2010). Type-B ARRs including ARR1, ARR10, and ARR12 directly activate the expression of WUS (Fig. 1D). Moreover, these ARRs directly repress the expression of YUCs, and indirectly promote WUS induction (Meng et al. 2017). Therefore, the feedback between WUS and cytokinin signaling Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020 aBIOTECH

aBIOTECHpathway,aswellasWUS-CLVfeedbackloop,producesSHOOTANDROOTSHARECOMMONPLAYERSaccurate positioning of the shoot stem cell niche cor-INTHEMAINTENANCEOFSTEMCELLIDENTITYrespondingtothemaximumof cytokinin response(Chickarmane et al.2012).STIMPY is another WUS-re-Root and shoot meristems share relatively conservedlatedhomeodomaintranscriptionfactor,whoseexpres-factorsforstemcell maintenance.Intherootmeristems,sion is identified to be induced by the cytokininthe quiescent center cells express the homeobox geneWOx5, which is a homologue of the WUS gene thatsignaling in the SAM of Arabidopsis (Skylar et al.2010;Wu et al.2005).Mutationof STIMPYresults in small andmaintains stemcells in the shoot meristem (Sarkar etal.differentiated SAM,which resembles wus mutantphe-2007).LossofW0x5functionintherootmeristemnotype (Wu et al. 2005).The expression of ARR5 iscauses terminal differentiation in distal stem cells andreduced in the stimpy mutants, showing that cytokininproximal meristem (Sarkar et al. 2007; Xu et al. 2019).responseis suppressedbySTIMPY.Therefore,STIMPYInterestingly,theexpression of theWUsfromtheWOx5coordinates with cytokinin signaling in the maintenancepromoter completelyrestores stem cells in the wox5ofshootstemcell activityrootmeristem.Conversely,ectopicexpression of wox5Thephytohormonecytokinin interactswiththe otherfromtheWuSpromoterrescuesprematureterminationsystemic signals and regulates shoot apical meristemof inflorescence meristems in the wus mutants, indi-size.Cytokininregulates SAMthroughkeytranscriptioncatingthatbothWUSand WOX5areinterchangeableinfactors including KNOTTED-LIKE (KNOXD)homeoboxcontrolling shoot and root apical meristems. This maybepartiallyaccountedforthefactthatbothWUSandtranscriptionfactors such asKNOTTED1 (KN1) inmaize(Vollbrecht et al.2000, 1991;Zinkgraf et al.2017)andWOX5 interact withHAM2(Zhou etal.2015).Therefore,STM inArabidopsis (Long et al.1996),both arerequiredtheArabidopsisHAM genesmayfunction as conservedinteracting cofactors with both WUS and WOx5 proteinsformaintainingtheproliferativestateofthemeristem-aticcells(Vollbrechtet al.20oo).Planthormonecyto-inshootorrootmeristems.kinin biosynthetic gene LONELY GUY (LOG) mutant has aAP2 domain transcription factor PLT3,which haswus-likephenotype,thus cytokinin signalingasa WUsbeenshownto controlrootapical stemcell identitypositional proximal to the shootapex cue of thegrowing(Galinha etal.2007),and its homologous proteinPLT5and PLT7 wererecentlyto showntoregulate shootArabidopsis shoot meristem through the antagonisticactivities of CLV3function (Chickarmaneet al.2012).apical meristem through regulating YUCCA1 (YUC1)andYUC4 modulated auxinbiosynthesis (Pinon etal.2013),Auxin functions are required inplant shoot stemcellmaintenance.InSAM,theintracellularauxin concentra-indicating that the local auxin biosynthesis is crucial forthe maintenance of shoot stem cell identity.The smalltion is regulated byPIN1 (Vernoux et al.2000), which issensedbythenuclearreceptorTRANSPORTINHIBITORsignaling peptide CLV3 was shown to bind to theRESPONSE1 (TIR1). The activated TIR1 combined withreceptor-like kinase protein (RLK) CLV1 in the shootauxin promoted theubiquitinationdegradation of auxinapical meristem tomaintainthestem cell fate (Ogawaet al. 2008). Recently, it was shown that the RLK proteinsignalinhibitingfactorAUX/IAA,and indirectlypromotedtheexpression ofARF genes (Kepinski and Leyser2005).CLV1 could act togetherwith themembrane-localizedA low-auxin zone is related to the shootapical meristem.RLKARABIDOPSISCRINKLY4(ACR4)tomodulatetheroot stem cell identity (Stahl et al. 2013). ACR4 canAuxinhasbeenshowntoinhibittheexpressionofARR7/15throughMP/ARF5tointerferewiththeWUS-CLV3interactwith and phosphorylatethetranscription factorW0X5 (Meyer et al.2015).feedbackloop,thusregulatingthehomeostasisof stemcells (Zhao et al. 2010).Mutations in the auxin signalingReactive oxygen species (ROS),including the super-componentARF3causesectopic cytokinin biosynthesisoxideanion, hydrogen peroxide, and the hydroxyl radi-viathemisexpressionISOPENTENYLTRANSFERASE5cal, and singlet oxygen, are formed in organelles during(AtiPT5) gene and disrupts the shoot stem cell activityelectrontransportreactions inphotosynthesisand res-and meristem maintenance (Chenget al.2013).MP/piration,and as byproducts of enzymatic reactions inARF5 has been also found to negatively regulate CLV3photorespiration and others metabolism.ROS plays anexpression by directly inhibiting DORNROSCHEN/important role in shootstem cell and root stem cellENHANCEROFSHOOTREGENERATION1(DRN/ESR1)identity (Wany et al. 2018; Yang et al. 2018). Redoxtranscription (Luo et al. 2018). Recently, WUS was foundmaster switches regulate organ growth, polarity,andtoregulateauxin signalingand responsepathways likeafloral development by integratingmajor hormone sig-variable resistor by regulating histone acetylation atnals and transcriptional networks inthe SAM (Schippersauxinpathwayloci,thusmaintainingthefateofstemet al.2016).OKINA KUKI(OKI1),which encodesacells in SAM (Ma et al. 2019).mitochondrialaspartyltRNAsynthetase(AspRS), Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020

pathway, as well as WUS-CLV feedback loop, produces accurate positioning of the shoot stem cell niche cor￾responding to the maximum of cytokinin response (Chickarmane et al. 2012). STIMPY is another WUS-re￾lated homeodomain transcription factor, whose expres￾sion is identified to be induced by the cytokinin signaling in the SAM of Arabidopsis (Skylar et al. 2010; Wu et al. 2005). Mutation of STIMPY results in small and differentiated SAM, which resembles wus mutant phe￾notype (Wu et al. 2005). The expression of ARR5 is reduced in the stimpy mutants, showing that cytokinin response is suppressed by STIMPY. Therefore, STIMPY coordinates with cytokinin signaling in the maintenance of shoot stem cell activity. The phytohormone cytokinin interacts with the other systemic signals and regulates shoot apical meristem size. Cytokinin regulates SAM through key transcription factors including KNOTTED-LIKE (KNOXI) homeobox transcription factors such as KNOTTED1 (KN1) in maize (Vollbrecht et al. 2000, 1991; Zinkgraf et al. 2017) and STM in Arabidopsis (Long et al. 1996), both are required for maintaining the proliferative state of the meristem￾atic cells (Vollbrecht et al. 2000). Plant hormone cyto￾kinin biosynthetic gene LONELY GUY (LOG) mutant has a wus-like phenotype, thus cytokinin signaling as a WUS positional proximal to the shoot apex cue of the growing Arabidopsis shoot meristem through the antagonistic activities of CLV3 function (Chickarmane et al. 2012). Auxin functions are required in plant shoot stem cell maintenance. In SAM, the intracellular auxin concentra￾tion is regulated by PIN1 (Vernoux et al. 2000), which is sensed by the nuclear receptor TRANSPORT INHIBITOR RESPONSE1 (TIR1). The activated TIR1 combined with auxin promoted the ubiquitination degradation of auxin signal inhibiting factor AUX/IAA, and indirectly promoted the expression of ARF genes (Kepinski and Leyser 2005). A low-auxin zone is related to the shoot apical meristem. Auxin has been shown to inhibit the expression of ARR7/ 15 through MP/ARF5 to interfere with the WUS-CLV3 feedback loop, thus regulating the homeostasis of stem cells (Zhao et al. 2010). Mutations in the auxin signaling component ARF3 causes ectopic cytokinin biosynthesis via the misexpression ISOPENTENYLTRANSFERASE5 (AtIPT5) gene and disrupts the shoot stem cell activity and meristem maintenance (Cheng et al. 2013). MP/ ARF5 has been also found to negatively regulate CLV3 expression by directly inhibiting DORNROSCHEN/ ENHANCER OF SHOOT REGENERATION 1 (DRN/ESR1) transcription (Luo et al. 2018). Recently, WUS was found to regulate auxin signaling and response pathways like a variable resistor by regulating histone acetylation at auxin pathway loci, thus maintaining the fate of stem cells in SAM (Ma et al. 2019). SHOOT AND ROOT SHARE COMMON PLAYERS IN THE MAINTENANCE OF STEM CELL IDENTITY Root and shoot meristems share relatively conserved factors for stem cell maintenance. In the root meristems, the quiescent center cells express the homeobox gene WOX5, which is a homologue of the WUS gene that maintains stem cells in the shoot meristem (Sarkar et al. 2007). Loss of WOX5 function in the root meristem causes terminal differentiation in distal stem cells and proximal meristem (Sarkar et al. 2007; Xu et al. 2019). Interestingly, the expression of the WUS from the WOX5 promoter completely restores stem cells in the wox5 root meristem. Conversely, ectopic expression of WOX5 from the WUS promoter rescues premature termination of inflorescence meristems in the wus mutants, indi￾cating that both WUS and WOX5 are interchangeable in controlling shoot and root apical meristems. This may be partially accounted for the fact that both WUS and WOX5 interact with HAM2 (Zhou et al. 2015). Therefore, the Arabidopsis HAM genes may function as conserved interacting cofactors with both WUS and WOX5 proteins in shoot or root meristems. AP2 domain transcription factor PLT3, which has been shown to control root apical stem cell identity (Galinha et al. 2007), and its homologous protein PLT5 and PLT7 were recently to shown to regulate shoot apical meristem through regulating YUCCA1 (YUC1) and YUC4 modulated auxin biosynthesis (Pinon et al. 2013), indicating that the local auxin biosynthesis is crucial for the maintenance of shoot stem cell identity. The small signaling peptide CLV3 was shown to bind to the receptor-like kinase protein (RLK) CLV1 in the shoot apical meristem to maintain the stem cell fate (Ogawa et al. 2008). Recently, it was shown that the RLK protein CLV1 could act together with the membrane-localized RLK ARABIDOPSIS CRINKLY4 (ACR4) to modulate the root stem cell identity (Stahl et al. 2013). ACR4 can interact with and phosphorylate the transcription factor WOX5 (Meyer et al. 2015). Reactive oxygen species (ROS), including the super￾oxide anion, hydrogen peroxide, and the hydroxyl radi￾cal, and singlet oxygen, are formed in organelles during electron transport reactions in photosynthesis and res￾piration, and as byproducts of enzymatic reactions in photorespiration and others metabolism. ROS plays an important role in shoot stem cell and root stem cell identity (Wany et al. 2018; Yang et al. 2018). Redox master switches regulate organ growth, polarity, and floral development by integrating major hormone sig￾nals and transcriptional networks in the SAM (Schippers et al. 2016). OKINA KUKI (OKI1), which encodes a mitochondrial aspartyl tRNA synthetase (AspRS), Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020 aBIOTECH

aBIOTECHmaintains the WUS-CLV3 feedback loop and SAM size bystudyisto establishtheregulatorynetworksof stemregulating Ros overaccumulation (Kitagawa et al.cell initiation and maintenanceto fully understand plant2019).The superoxide anion, which is enriched indevelopmentinresponseto endogenousdevelopmentalcentral zone of shoot stem cells,could activate WUS andcues and exogenous environmental cues.maintain stemness,whereashydrogen peroxidecanInbothSAMandRAM,hormonessuchascytokininpromote stem cell differentiation and negatively regu-and auxin play important roles in both shoot and rootlates superoxide anion biosynthesisin stem cells.stem cell niche function,specification,and differentia-Therefore, the balance between superoxide anion andtion through cell autonomous or non-autonomoushydrogen peroxide is essential for the regulation ofmanners.Thecooperativeactionofplanthormonesandshoot stem cell maintenance and differentiation (Zengtranscriptionfactorsdeterminesthebalanceof stem celletal.2017).Similartoshoot,R0Salsoactasmastermaintenance and organ formation in plant meristem.regulators in root SCN maintenance. A bHLH tran-Besides hormones, multiple common signals such asscription factor, UPBEAT1 (UPB1), directly regulates theROS and peptides were identified as necessary to posi-expression ofa set of peroxidases between thezones oftion and to maintain the shoot and root stem cell niches,cell proliferationand thezoneof cell elongationwhereindicating conserved mechanismsintheshootand rootdifferentiation begins by establishing agradient of ROS,stem cell niche function.Given that the similarities ofthus controls thetransition fromproliferation to dif-theregulatorymechanisms inthe shootand root stemferentiation (Tsukagoshi et al.2010).The Arabidopsiscell niche, it is consistent with paleobotanical viewsthatP-loopNTPaseencodedbyAPP1affectsrootOCandthe root evolved from shoot (Szovenyi et al. 2019).distal stem cell identity through maintaining root ROSHowever,the nature of these conserved mechanisms ishomeostasis.APP1 positively regulates the expressionstill not completelyunderstood.of SCR and SHR by regulating ROS signaling, which isMore recently,live-imaging technology has enabledessentialforthemaintenanceofrootQCanddistalstemhigh-resolutionspatio-temporalanalysisof genecell identity (Yu et al.2016).TheDPR2 gene encodesexpression patterns, which is useful to analyze thephosphoethanolamineN-methyltransferase1 (PEAMT1)spatial parameters of hormonal and transcriptionalthat catalyzes phosphocholine biosynthesis in Ara-regulatory modules (Sijacic and Liu2010).Furthermore,bidopsis.LosS-of-functionofDPR2/PEAMT1resultedincomputational methodsforboth image analysis andRAM consumption by affecting root stem cell niche,quantitative modeling will provide newinsights intothedivision zone, and elongation and differentiation zonecomplex and intricate models of hormone regulated(EDZ),which wereresultfrom thealtered ROS andstem-cell initiation and maintenance in the SAM andRAM.auxinhomeostasis (Zou etal.2019).ROSsignalingcouldbe also interpretedthrough ROS-responsivefactors suchSingle cell RNA sequencing (scRNA-seq) technologyas ERF transcription factors ERF115, ERF114, andcan yield high-resolution cell-type-specific expressionERF109 to maintain root SCN identity (Kong et al.2018).signatures that reveal new cell types and the develop-Together, all these results suggest that ROS are involvedmental trajectories of stem cells at the single-cell levelinthemaintenanceofbothshootstemcellandroot(ZhangandLiu2019).Using scRNA-seq,recent studieshaverevealed the cellular heterogeneity and the devel-stemcell identity.opmental trajectory of root.It has been reported thatthethree-dimensional(3D)genomeorganizationplaysCONCLUDINGREMARKSimportant roles during stem cell maintenanceand dif-ferentiation (Zujur etal.2017).Inplant cells,thewhole-Plant stem cells havea strong abilitytorenewthem-genomechromatinstructuresofmanyspeciessuchasselves and to generate daughter cells to produce newArabidopsis, rice,maize and tomato havebeen unveiledtissues.The plasticity of stem cells allows plants tousing Hi-C technology.Thus,the combination of scRNA-adapt their shape in response todevelopmental,physi-seg with Hi-C technology and all the other new devel-cal,and environmental cues(Wierzbaand Tax2013;Xuoped toolsmayhelpus to investigatethelogic of rootetal.2018,2019;Yuetal.2019a).Thebalancebetweenandshootstemcell functioninthefuture.the proliferation and differentiation of stemcellsAcknowledgements We apologize to our colleagues whose workdetermines their populations in the meristem. Thecould not be cited in this review because of space limitations.Thiselaborategeneticregulatorypathwaythatregulatesthework is supported by the Shandong Province Natural Scienceinitiation and maintenance of shoot and root stem cellsFoundation of Major Basic Research Program(2017C03),byis amajor area of interest in plant developmentalQingdao's Leading Technology Innovator Project, and by Youthresearch. Therefore, a significant challenge for future Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020

maintains the WUS-CLV3 feedback loop and SAM size by regulating ROS overaccumulation (Kitagawa et al. 2019). The superoxide anion, which is enriched in central zone of shoot stem cells, could activate WUS and maintain stemness, whereas hydrogen peroxide can promote stem cell differentiation and negatively regu￾lates superoxide anion biosynthesis in stem cells. Therefore, the balance between superoxide anion and hydrogen peroxide is essential for the regulation of shoot stem cell maintenance and differentiation (Zeng et al. 2017). Similar to shoot, ROS also act as master regulators in root SCN maintenance. A bHLH tran￾scription factor, UPBEAT1 (UPB1), directly regulates the expression of a set of peroxidases between the zones of cell proliferation and the zone of cell elongation where differentiation begins by establishing a gradient of ROS, thus controls the transition from proliferation to dif￾ferentiation (Tsukagoshi et al. 2010). The Arabidopsis P-loop NTPase encoded by APP1 affects root QC and distal stem cell identity through maintaining root ROS homeostasis. APP1 positively regulates the expression of SCR and SHR by regulating ROS signaling, which is essential for the maintenance of root QC and distal stem cell identity (Yu et al. 2016). The DPR2 gene encodes phosphoethanolamine N-methyltransferase 1 (PEAMT1) that catalyzes phosphocholine biosynthesis in Ara￾bidopsis. Loss-of-function of DPR2/PEAMT1 resulted in RAM consumption by affecting root stem cell niche, division zone, and elongation and differentiation zone (EDZ), which were result from the altered ROS and auxin homeostasis (Zou et al. 2019). ROS signaling could be also interpreted through ROS-responsive factors such as ERF transcription factors ERF115, ERF114, and ERF109 to maintain root SCN identity (Kong et al. 2018). Together, all these results suggest that ROS are involved in the maintenance of both shoot stem cell and root stem cell identity. CONCLUDING REMARKS Plant stem cells have a strong ability to renew them￾selves and to generate daughter cells to produce new tissues. The plasticity of stem cells allows plants to adapt their shape in response to developmental, physi￾cal, and environmental cues (Wierzba and Tax 2013; Xu et al. 2018, 2019; Yu et al. 2019a). The balance between the proliferation and differentiation of stem cells determines their populations in the meristem. The elaborate genetic regulatory pathway that regulates the initiation and maintenance of shoot and root stem cells is a major area of interest in plant developmental research. Therefore, a significant challenge for future study is to establish the regulatory networks of stem cell initiation and maintenance to fully understand plant development in response to endogenous developmental cues and exogenous environmental cues. In both SAM and RAM, hormones such as cytokinin and auxin play important roles in both shoot and root stem cell niche function, specification, and differentia￾tion through cell autonomous or non-autonomous manners. The cooperative action of plant hormones and transcription factors determines the balance of stem cell maintenance and organ formation in plant meristem. Besides hormones, multiple common signals such as ROS and peptides were identified as necessary to posi￾tion and to maintain the shoot and root stem cell niches, indicating conserved mechanisms in the shoot and root stem cell niche function. Given that the similarities of the regulatory mechanisms in the shoot and root stem cell niche, it is consistent with paleobotanical views that the root evolved from shoot (Szovenyi et al. 2019). However, the nature of these conserved mechanisms is still not completely understood. More recently, live-imaging technology has enabled high-resolution spatio-temporal analysis of gene expression patterns, which is useful to analyze the spatial parameters of hormonal and transcriptional regulatory modules (Sijacic and Liu 2010). Furthermore, computational methods for both image analysis and quantitative modeling will provide new insights into the complex and intricate models of hormone regulated stem-cell initiation and maintenance in the SAM and RAM. Single cell RNA sequencing (scRNA-seq) technology can yield high-resolution cell-type-specific expression signatures that reveal new cell types and the develop￾mental trajectories of stem cells at the single-cell level (Zhang and Liu 2019). Using scRNA-seq, recent studies have revealed the cellular heterogeneity and the devel￾opmental trajectory of root. It has been reported that the three-dimensional (3D) genome organization plays important roles during stem cell maintenance and dif￾ferentiation (Zujur et al. 2017). In plant cells, the whole￾genome chromatin structures of many species such as Arabidopsis, rice, maize and tomato have been unveiled using Hi-C technology. Thus, the combination of scRNA￾seq with Hi-C technology and all the other new devel￾oped tools may help us to investigate the logic of root and shoot stem cell function in the future. Acknowledgements We apologize to our colleagues whose work could not be cited in this review because of space limitations. This work is supported by the Shandong Province Natural Science Foundation of Major Basic Research Program (2017C03), by Qingdao’s Leading Technology Innovator Project, and by Youth Agricultural Information Institute, Chinese Academy of Agricultural Sciences 2020 aBIOTECH

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