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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aida M, Ishida T, Tasaka M (1999) Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126:1563–1570
Aida M et al (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120. https://doi.org/10.1016/j.cell.2004.09.018
Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT, Aeschbacher RA (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70
Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602. https://doi.org/10.1016/s0092-8674(03)00924-3
Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–619. https://doi.org/10.1126/science.289.5479.617
Cheng ZJ et al (2013) Pattern of auxin and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by AUXIN RESPONSE FACTOR3. Plant Physiol 161:240–251. https://doi.org/10.1104/pp.112.203166
Chickarmane VS, Gordon SP, Tarr PT, Heisler MG, Meyerowitz EM (2012) Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. Proc Natl Acad Sci USA 109:4002–4007. https://doi.org/10.1073/pnas.1200636109
Crawford BC, Sewell J, Golembeski G, Roshan C, Long JA, Yanofsky MF (2015) Plant development. Genetic control of distal stem cell fate within root and embryonic meristems. Science 347:655–659. https://doi.org/10.1126/science.aaa0196
Dai X, Liu Z, Qiao M, Li J, Li S, Xiang F (2017) ARR12 promotes de novo shoot regeneration in Arabidopsisthaliana via activation of WUSCHEL expression. J Integr Plant Biol 59:747–758. https://doi.org/10.1111/jipb.12567
Daum G, Medzihradszky A, Suzaki T, Lohmann JU (2014) A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis. Proc Natl Acad Sci USA 111:14619–14624. https://doi.org/10.1073/pnas.1406446111
De Smet I (2010) Multimodular auxin response controls lateral root development in Arabidopsis. Plant Signal Behav 5:580–582. https://doi.org/10.4161/psb.11495
Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17:678–682. https://doi.org/10.1016/j.cub.2007.02.047
Dello Ioio R et al (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:1380–1384. https://doi.org/10.1126/science.1164147
Dello Ioio R et al (2012) A PHABULOSA/cytokinin feedback loop controls root growth in Arabidopsis. Curr Biol 22:1699–1704. https://doi.org/10.1016/j.cub.2012.07.005
Di Mambro R et al (2017) Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root. Proc Natl Acad Sci USA 114:E7641–E7649. https://doi.org/10.1073/pnas.1705833114
Di Mambro R et al (2019) The lateral root cap acts as an auxin sink that controls meristem size. Curr Biol 29(1199–1205):e1194. https://doi.org/10.1016/j.cub.2019.02.022
Ding Z, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc Natl Acad Sci USA 107:12046–12051. https://doi.org/10.1073/pnas.1000672107
Dinneny JR, Benfey PN (2008) Plant stem cell niches: standing the test of time. Cell 132:553–557. https://doi.org/10.1016/j.cell.2008.02.001
Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsisthaliana root. Development 119:71–84
Forzani C, Aichinger E, Sornay E, Willemsen V, Laux T, Dewitte W, Murray JA (2014) WOX5 suppresses CYCLIN D activity to establish quiescence at the center of the root stem cell niche. Curr Biol 24:1939–1944. https://doi.org/10.1016/j.cub.2014.07.019
Friml J et al (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306:862–865. https://doi.org/10.1126/science.1100618
Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057. https://doi.org/10.1038/nature06206
Galli M, Gallavotti A (2016) Expanding the regulatory network for meristem size in plants. Trends Genet 32:372–383. https://doi.org/10.1016/j.tig.2016.04.001
Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM (2009) Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc Natl Acad Sci USA 106:16529–16534. https://doi.org/10.1073/pnas.0908122106
Grieneisen VA, Xu J, Maree AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013. https://doi.org/10.1038/nature06215
Hamann T, Benkova E, Baurle I, Kientz M, Jurgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–1615. https://doi.org/10.1101/gad.229402
Heidstra R, Sabatini S (2014) Plant and animal stem cells: similar yet different. Nat Rev Mol Cell Biol 15:301–312. https://doi.org/10.1038/nrm3790
Hibara K, Karim MR, Takada S, Taoka K, Furutani M, Aida M, Tasaka M (2006) Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell 18:2946–2957. https://doi.org/10.1105/tpc.106.045716
Hwang I, Sheen J, Muller B (2012) Cytokinin signaling networks. Annu Rev Plant Biol 63:353–380. https://doi.org/10.1146/annurev-arplant-042811-105503
Jasinski S et al (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15:1560–1565. https://doi.org/10.1016/j.cub.2005.07.023
Jeong S, Bayer M, Lukowitz W (2011) Taking the very first steps: from polarity to axial domains in the early Arabidopsis embryo. J Exp Bot 62:1687–1697. https://doi.org/10.1093/jxb/erq398
Jiang K, Feldman LJ (2005) Regulation of root apical meristem development. Annu Rev Cell Dev Biol 21:485–509. https://doi.org/10.1146/annurev.cellbio.21.122303.114753
Jurgens G, Torres Ruiz RA, Berleth T (1994) Embryonic pattern formation in flowering plants. Annu Rev Genet 28:351–371. https://doi.org/10.1146/annurev.ge.28.120194.002031
Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451. https://doi.org/10.1038/nature03542
Kitagawa M, Balkunde R, Bui H, Jackson D (2019) An aminoacyl tRNA synthetase, OKI1 is required for proper shoot meristem size in Arabidopsis. Plant Cell Physiol 60:2597–2608. https://doi.org/10.1093/pcp/pcz153
Kong X et al (2018) PHB3 maintains root stem cell niche identity through ROS-responsive AP2/ERF transcription factors in Arabidopsis. Cell Rep 22:1350–1363. https://doi.org/10.1016/j.celrep.2017.12.105
Lau S, Jurgens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant Cell 20:1738–1746. https://doi.org/10.1105/tpc.108.060418
Leibfried A et al (2005) WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438:1172–1175. https://doi.org/10.1038/nature04270
Liu C et al (2013) Phosphatidylserine synthase 1 is required for inflorescence meristem and organ development in Arabidopsis. J Integr Plant Biol 55:682–695. https://doi.org/10.1111/jipb.12045
Liu Y, Xu M, Liang N, Zheng Y, Yu Q, Wu S (2017) Symplastic communication spatially directs local auxin biosynthesis to maintain root stem cell niche in Arabidopsis. Proc Natl Acad Sci USA 114:4005–4010. https://doi.org/10.1073/pnas.1616387114
Lofke C, Dunser K, Kleine-Vehn J (2013) Epidermal patterning genes impose non-cell autonomous cell size determination and have additional roles in root meristem size control. J Integr Plant Biol 55:864–875. https://doi.org/10.1111/jipb.12097
Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69. https://doi.org/10.1038/379066a0
Long JA, Woody S, Poethig S, Meyerowitz EM, Barton MK (2002) Transformation of shoots into roots in Arabidopsis embryos mutant at the TOPLESS locus. Development 129:2797–2806
Long JA, Ohno C, Smith ZR, Meyerowitz EM (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312:1520–1523. https://doi.org/10.1126/science.1123841
Luo L, Zeng J, Wu H, Tian Z, Zhao Z (2018) A molecular framework for auxin-controlled homeostasis of shoot stem cells in Arabidopsis. Mol Plant 11:899–913. https://doi.org/10.1016/j.molp.2018.04.006
Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P, Barton MK (1999) The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126:469–481
Ma Y et al (2019) WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis. Nat Commun 10:5093. https://doi.org/10.1038/s41467-019-13074-9
Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y (2010) Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329:1065–1067. https://doi.org/10.1126/science.1191132
Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815. https://doi.org/10.1016/s0092-8674(00)81703-1
Meng WJ et al (2017) Type-B ARABIDOPSIS RESPONSE REGULATORs specify the shoot stem cell niche by dual regulation of WUSCHEL. Plant Cell 29:1357–1372. https://doi.org/10.1105/tpc.16.00640
Meyer MR, Shah S, Zhang J, Rohrs H, Rao AG (2015) Evidence for intermolecular interactions between the intracellular domains of the Arabidopsis receptor-like kinase ACR4, its homologs and the Wox5 transcription factor. PLoS ONE 10:e0118861. https://doi.org/10.1371/journal.pone.0118861
Moubayidin L, Perilli S, Dello Ioio R, Di Mambro R, Costantino P, Sabatini S (2010) The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr Biol 20:1138–1143. https://doi.org/10.1016/j.cub.2010.05.035
Moubayidin L et al (2013) Spatial coordination between stem cell activity and cell differentiation in the root meristem. Dev Cell 26:405–415. https://doi.org/10.1016/j.devcel.2013.06.025
Moussian B, Schoof H, Haecker A, Jurgens G, Laux T (1998) Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J 17:1799–1809. https://doi.org/10.1093/emboj/17.6.1799
Muller B, Sheen J (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453:1094–1097. https://doi.org/10.1038/nature06943
Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294. https://doi.org/10.1126/science.1150083
Perales M, Rodriguez K, Snipes S, Yadav RK, Diaz-Mendoza M, Reddy GV (2016) Threshold-dependent transcriptional discrimination underlies stem cell homeostasis. Proc Natl Acad Sci USA 113:E6298–E6306. https://doi.org/10.1073/pnas.1607669113
Perilli S, Di Mambro R, Sabatini S (2012) Growth and development of the root apical meristem. Curr Opin Plant Biol 15:17–23. https://doi.org/10.1016/j.pbi.2011.10.006
Pi L et al (2015) Organizer-derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4 expression. Dev Cell 33:576–588. https://doi.org/10.1016/j.devcel.2015.04.024
Pinon V, Prasad K, Grigg SP, Sanchez-Perez GF, Scheres B (2013) Local auxin biosynthesis regulation by PLETHORA transcription factors controls phyllotaxis in Arabidopsis. Proc Natl Acad Sci USA 110:1107–1112. https://doi.org/10.1073/pnas.1213497110
Rademacher EH et al (2012) Different auxin response machineries control distinct cell fates in the early plant embryo. Dev Cell 22:211–222. https://doi.org/10.1016/j.devcel.2011.10.026
Roodbarkelari F, Du F, Truernit E, Laux T (2015) ZLL/AGO10 maintains shoot meristem stem cells during Arabidopsis embryogenesis by down-regulating ARF2-mediated auxin response. BMC Biol 13:74. https://doi.org/10.1186/s12915-015-0180-y
Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17:354–358. https://doi.org/10.1101/gad.252503
Saiga S et al (2008) The Arabidopsis OBERON1 and OBERON2 genes encode plant homeodomain finger proteins and are required for apical meristem maintenance. Development 135:1751–1759. https://doi.org/10.1242/dev.014993
Saiga S, Moller B, Watanabe-Taneda A, Abe M, Weijers D, Komeda Y (2012) Control of embryonic meristem initiation in Arabidopsis by PHD-finger protein complexes. Development 139:1391–1398. https://doi.org/10.1242/dev.074492
Sarkar AK et al (2007) Conserved factors regulate signalling in Arabidopsisthaliana shoot and root stem cell organizers. Nature 446:811–814. https://doi.org/10.1038/nature05703
Sato-Izawa K et al (2012) DWARF50 (D50), a rice (Oryzasativa L.) gene encoding inositol polyphosphate 5-phosphatase, is required for proper development of intercalary meristem. Plant Cell Environ 35:2031–2044. https://doi.org/10.1111/j.1365-3040.2012.02534.x
Schippers JH, Foyer CH, van Dongen JT (2016) Redox regulation in shoot growth, SAM maintenance and flowering. Curr Opin Plant Biol 29:121–128. https://doi.org/10.1016/j.pbi.2015.11.009
Schlereth A et al (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916. https://doi.org/10.1038/nature08836
Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644. https://doi.org/10.1016/s0092-8674(00)80700-x
Sijacic P, Liu Z (2010) Novel insights from live-imaging in shoot meristem development. J Integr Plant Biol 52:393–399. https://doi.org/10.1111/j.1744-7909.2010.00941.x
Skylar A, Hong F, Chory J, Weigel D, Wu X (2010) STIMPY mediates cytokinin signaling during shoot meristem establishment in Arabidopsis seedlings. Development 137:541–549. https://doi.org/10.1242/dev.041426
Smetana O et al (2019) High levels of auxin signalling define the stem-cell organizer of the vascular cambium. Nature 565:485–489. https://doi.org/10.1038/s41586-018-0837-0
Song X, Guo P, Li C, Liu CM (2010) The cysteine pairs in CLV2 are not necessary for sensing the CLV3 peptide in shoot and root meristems. J Integr Plant Biol 52:774–781. https://doi.org/10.1111/j.1744-7909.2010.00978.x
Spinelli SV, Martin AP, Viola IL, Gonzalez DH, Palatnik JF (2011) A mechanistic link between STM and CUC1 during Arabidopsis development. Plant Physiol 156:1894–1904. https://doi.org/10.1104/pp.111.177709
Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19:909–914. https://doi.org/10.1016/j.cub.2009.03.060
Stahl Y et al (2013) Moderation of Arabidopsis root sternness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr Biol 23:362–371. https://doi.org/10.1016/j.cub.2013.01.045
Su YH, Liu YB, Bai B, Zhang XS (2014) Establishment of embryonic shoot-root axis is involved in auxin and cytokinin response during Arabidopsis somatic embryogenesis. Front Plant Sci 5:792. https://doi.org/10.3389/fpls.2014.00792
Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386. https://doi.org/10.1126/science.1151461
Szovenyi P, Waller M, Kirbis A (2019) Evolution of the plant body plan. Curr Top Dev Biol 131:1–34. https://doi.org/10.1016/bs.ctdb.2018.11.005
Takada S, Hibara K, Ishida T, Tasaka M (2001) The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128:1127–1135
Thomas CL, Schmidt D, Bayer EM, Dreos R, Maule AJ (2009) Arabidopsis plant homeodomain finger proteins operate downstream of auxin accumulation in specifying the vasculature and primary root meristem. Plant J 59:426–436. https://doi.org/10.1111/j.1365-313X.2009.03874.x
Tian H et al (2014) WOX5-IAA17 feedback circuit-mediated cellular auxin response is crucial for the patterning of root stem cell niches in Arabidopsis. Mol Plant 7:277–289. https://doi.org/10.1093/mp/sst118
Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616. https://doi.org/10.1016/j.cell.2010.10.020
Tucker MR, Hinze A, Tucker EJ, Takada S, Jurgens G, Laux T (2008) Vascular signalling mediated by ZWILLE potentiates WUSCHEL function during shoot meristem stem cell development in the Arabidopsis embryo. Development 135:2839–2843. https://doi.org/10.1242/dev.023648
Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J (2000) PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. Development 127:5157–5165
Vollbrecht E, Veit B, Sinha N, Hake S (1991) The developmental gene knotted-1 is a member of a maize homeobox gene family. Nature 350:241–243. https://doi.org/10.1038/350241a0
Vollbrecht E, Reiser L, Hake S (2000) Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1. Development 127:3161–3172
Wang Z, Mao JL, Zhao YJ, Li CY, Xiang CB (2015) L-Cysteine inhibits root elongation through auxin/PLETHORA and SCR/SHR pathway in Arabidopsisthaliana. J Integr Plant Biol 57:186–197. https://doi.org/10.1111/jipb.12213
Wany A, Foyer CH, Gupta KJ (2018) Nitrate, NO and ROS signaling in stem cell homeostasis. Trends Plant Sci 23:1041–1044. https://doi.org/10.1016/j.tplants.2018.09.010
Weijers D et al (2005) Maintenance of embryonic auxin distribution for apical-basal patterning by PIN-FORMED-dependent auxin transport in Arabidopsis. Plant Cell 17:2517–2526. https://doi.org/10.1105/tpc.105.034637
Weijers D, Schlereth A, Ehrismann JS, Schwank G, Kientz M, Jurgens G (2006) Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev Cell 10:265–270. https://doi.org/10.1016/j.devcel.2005.12.001
Wierzba MP, Tax FE (2013) Notes from the underground: receptor-like kinases in Arabidopsis root development. J Integr Plant Biol 55:1224–1237. https://doi.org/10.1111/jipb.12088
Willmann MR (2000) CLV1 and CLV3: negative regulators of SAM stem cell accumulation. Trends Plant Sci 5:416. https://doi.org/10.1016/s1360-1385(00)01763-5
Wolters H, Jurgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet 10:305–317. https://doi.org/10.1038/nrg2558
Wu X, Dabi T, Weigel D (2005) Requirement of homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance. Curr Biol 15:436–440. https://doi.org/10.1016/j.cub.2004.12.079
Xu Y et al (2018) CYSTM, a novel non-secreted cysteine-rich peptide family, involved in environmental stresses in Arabidopsisthaliana. Plant Cell Physiol 59:423–438. https://doi.org/10.1093/pcp/pcx202
Xu M et al (2019) Intersected functional zone of transcriptional regulators patterns stemness within stem cell niche of root apical meristem. J Integr Plant Biol. https://doi.org/10.1111/jipb.12881
Yanai O et al (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol 15:1566–1571. https://doi.org/10.1016/j.cub.2005.07.060
Yang S, Yu Q, Zhang Y, Jia Y, Wan S, Kong X, Ding Z (2018) ROS: the fine-tuner of plant stem cell fate. Trends Plant Sci 23:850–853. https://doi.org/10.1016/j.tplants.2018.07.010
Yang G, Yu Z, Gao L, Zheng C (2019) SnRK2s at the crossroads of growth and stress responses. Trends Plant Sci 24:672–676. https://doi.org/10.1016/j.tplants.2019.05.010
Yao Q et al (2019) High efficient expression and purification of human epidermal growth factor in Arachishypogaea L. Int J Mol Sci. https://doi.org/10.3390/ijms20082045
Yu Q, Tian H, Yue K, Liu J, Zhang B, Li X, Ding Z (2016) A P-loop NTPase regulates quiescent center cell division and distal stem cell identity through the regulation of ROS homeostasis in Arabidopsis root. PLoS Genet 12:e1006175. https://doi.org/10.1371/journal.pgen.1006175
Yu Z et al (2019a) The importance of conserved serine for C-terminally encoded peptides function exertion in apple. Int J Mol Sci. https://doi.org/10.3390/ijms20030775
Yu Z et al (2019b) The Brassicaceae-specific secreted peptides, STMPs, function in plant growth and pathogen defense. J Integr Plant Biol. https://doi.org/10.1111/jipb.12817
Yu Z et al (2019c) CEPR2 phosphorylates and accelerates the degradation of PYR/PYLs in Arabidopsis. J Exp Bot 70:5457–5469. https://doi.org/10.1093/jxb/erz302
Zeng J, Dong Z, Wu H, Tian Z, Zhao Z (2017) Redox regulation of plant stem cell fate. EMBO J 36:2844–2855. https://doi.org/10.15252/embj.201695955
Zhang JJ, Xue HW (2013) OsLEC1/OsHAP3E participates in the determination of meristem identity in both vegetative and reproductive developments of rice. J Integr Plant Biol 55:232–249. https://doi.org/10.1111/jipb.12025
Zhang X, Liu L (2019) Applications of single cell RNA sequencing to research of stem cells. World J Stem Cells 11:722–728. https://doi.org/10.4252/wjsc.v11.i10.722
Zhang Y, Jiao Y, Liu Z, Zhu YX (2015) ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells. Nat Commun 6:6003. https://doi.org/10.1038/ncomms7003
Zhang Z, Tucker E, Hermann M, Laux T (2017) A molecular framework for the embryonic initiation of shoot meristem stem cells. Dev Cell 40(3):264–277. https://doi.org/10.1016/j.devcel.2017.01.002
Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A, Schultheiss SJ, Lohmann JU (2010) Hormonal control of the shoot stem-cell niche. Nature 465:1089–1092. https://doi.org/10.1038/nature09126
Zhao Q, Wu Y, Gao L, Ma J, Li CY, Xiang CB (2014) Sulfur nutrient availability regulates root elongation by affecting root indole-3-acetic acid levels and the stem cell niche. J Integr Plant Biol 56:1151–1163. https://doi.org/10.1111/jipb.12217
Zhou W et al (2010) Arabidopsis tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22:3692–3709. https://doi.org/10.1105/tpc.110.075721
Zhou Y et al (2015) Control of plant stem cell function by conserved interacting transcriptional regulators. Nature 517:377–380. https://doi.org/10.1038/nature13853
Zinkgraf M, Gerttula S, Groover A (2017) Transcript profiling of a novel plant meristem, the monocot cambium. J Integr Plant Biol 59:436–449. https://doi.org/10.1111/jipb.12538
Zou Y, Zhang X, Tan Y, Huang JB, Zheng Z, Tao LZ (2019) Phosphoethanolamine N-methyltransferase 1 contributes to maintenance of root apical meristem by affecting ROS and auxin-regulated cell differentiation in Arabidopsis. New Phytol 224:258–273. https://doi.org/10.1111/nph.16028
Zujur D, Kanke K, Lichtler AC, Hojo H, Chung UI, Ohba S (2017) Three-dimensional system enabling the maintenance and directed differentiation of pluripotent stem cells under defined conditions. Sci Adv 3:e1602875. https://doi.org/10.1126/sciadv.1602875
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 Interdisciplinary Science and Innovative Research Groups of Shandong University (Grant No. 2020QNQT014).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Wang, J., Su, Y., Kong, X. et al. Initiation and maintenance of plant stem cells in root and shoot apical meristems. aBIOTECH 1, 194–204 (2020). https://doi.org/10.1007/s42994-020-00020-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42994-020-00020-3