Please wait a minute...
Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front Biol    2010, Vol. 5 Issue (5) : 417-423    https://doi.org/10.1007/s11515-010-0880-1
REVIEW
Plant stem cells and their regulations in shoot apical meristems
Chun-Ming LIU(), Yuxin HU()
Center for Signal Transduction & Metabolomics, Key Laboratory of Photosynthesis and Environmental Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
 Download: PDF(312 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

Stem cells in plants, established during embryogenesis, are located in the centers of the shoot apical meristem (SAM) and the root apical meristem (RAM). Stem cells in SAM have a capacity to renew themselves and to produce new organs and tissues indefinitely. Although fully differentiated organs such as leaves do not contain stem cells, cells in such organs do have the capacity to re-establish new stem cells, especially under the induction of phytohormones in vitro. Cytokinin and auxin are critical in creating position signals in the SAM to maintain the stem cell organizing center and to position the new organ primordia, respectively. This review addresses the distinct features of plant stem cells and focuses on how stem cell renewal and differentiation are regulated in SAMs.

Keywords plant      stem cell      shoot apical meristem      root apical meristem     
Corresponding Author(s): LIU Chun-Ming,Email:cmliu@ibcas.ac.cn; HU Yuxin,Email:huyuxin@ibcas.ac.cn   
Issue Date: 01 October 2010
 Cite this article:   
Chun-Ming LIU,Yuxin HU. Plant stem cells and their regulations in shoot apical meristems[J]. Front Biol, 2010, 5(5): 417-423.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-010-0880-1
https://academic.hep.com.cn/fib/EN/Y2010/V5/I5/417
Fig.1  Structures of shoot apical meristem (SAM, upper) and root apical meristem (RAM, below) are shown. Stem cells (in cyan) in SAM are cells located in the central zone, occupying the L1, L2 and upper L3 layers; while stem cells in RAM are cells with direct contacts with stem cell organizing center. Stem cell organizing center (in red) in SAM is located in the L3 layer of the central zone; the organizing center in RAM is quiescent center, which usually contains 4 cells in Arabidopsis. Stem cells and the cells in organizing center are usually vacuolated and slowly dividable.
Fig.1  Structures of shoot apical meristem (SAM, upper) and root apical meristem (RAM, below) are shown. Stem cells (in cyan) in SAM are cells located in the central zone, occupying the L1, L2 and upper L3 layers; while stem cells in RAM are cells with direct contacts with stem cell organizing center. Stem cell organizing center (in red) in SAM is located in the L3 layer of the central zone; the organizing center in RAM is quiescent center, which usually contains 4 cells in Arabidopsis. Stem cells and the cells in organizing center are usually vacuolated and slowly dividable.
Fig.2  The phenotypes of the () mutants. The photos show the size of SAMs (left) and the shape of siliques (right) of wild type (A) and mutant (B). Note the greatly enlarged SAM and increased carpel number in .
Fig.2  The phenotypes of the () mutants. The photos show the size of SAMs (left) and the shape of siliques (right) of wild type (A) and mutant (B). Note the greatly enlarged SAM and increased carpel number in .
Fig.3  Schematic representation of the stem cell regulation machinery in shoot apical meristem. Stem cells (cyan) are marked by the expression of , while stem cell organizing center is marked by the expression of (red). The mobile peptide ligand CLV3 produced by stem cells provides a stem cell-restricting signal that is perceived by CLV1 receptor kinases in cells below. The signal is then delivered to over-lapping stem cell organizing center cells to repress the expression of . WUS is a stem cell-promoting signal that enhances the expression of . In such, CLV and WUS together build a negative feedback regulation loop to maintain the proper number of stem cells in SAM. A high level of cytokinin (pink) located in the center of SAM may provide a position signal to maintain the WUS domain.
Fig.3  Schematic representation of the stem cell regulation machinery in shoot apical meristem. Stem cells (cyan) are marked by the expression of , while stem cell organizing center is marked by the expression of (red). The mobile peptide ligand CLV3 produced by stem cells provides a stem cell-restricting signal that is perceived by CLV1 receptor kinases in cells below. The signal is then delivered to over-lapping stem cell organizing center cells to repress the expression of . WUS is a stem cell-promoting signal that enhances the expression of . In such, CLV and WUS together build a negative feedback regulation loop to maintain the proper number of stem cells in SAM. A high level of cytokinin (pink) located in the center of SAM may provide a position signal to maintain the WUS domain.
Fig.4  The CLV3-WUS signal transduction pathway. CLV3 preproproteins produced by stem cells are secreted to intercellular spaces and then cleaved to a small peptide, further processed by SOL1 carboxylpeptidases, modified by hydroxylation and glycosylation. The peptide signal is most likely perceived by either a CLV1 homodimer and a CLV2-CRN heterodimer or a multimeric complex containing CLV1, CLV2 and CRN, which then repress the expression of in stem cell organizing center cells.
Fig.4  The CLV3-WUS signal transduction pathway. CLV3 preproproteins produced by stem cells are secreted to intercellular spaces and then cleaved to a small peptide, further processed by SOL1 carboxylpeptidases, modified by hydroxylation and glycosylation. The peptide signal is most likely perceived by either a CLV1 homodimer and a CLV2-CRN heterodimer or a multimeric complex containing CLV1, CLV2 and CRN, which then repress the expression of in stem cell organizing center cells.
1 Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh Y S, Amasino R, Scheres B (2004). The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell , 119(1): 109–120
2 Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell , 115(5): 591–602
3 Brand U, Fletcher J C, Hobe M, Meyerowitz E M, Simon R (2000). Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science , 289(5479): 617–619
doi: 10.1126/science.289.5479.617
4 Casamitjana-Martínez E, Hofhuis H F, Xu J, Liu C M, Heidstra R, Scheres B (2003). Root-specific CLE19 overexpression and the sol/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Curr Biol , 13(16): 1435–1441
doi: 10.1016/S0960-9822(03)00533-5
5 Chu H, Qian Q, Liang W, Yin C, Tan H, Yao X, Yuan Z, Yang J, Huang H, Luo D, Ma H, Zhang D (2006). The FLORAL ORGAN NUMBER4 organ number4 gene encoding a putative ortholog of Arabidopsis CLAVATA3 regulates apical meristem size in rice. Plant Physiol , 142(3): 1039–1052
doi: 10.1104/pp.106.086736
6 Clark S E, Williams R W, Meyerowitz E M (1997). The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell , 89(4): 575–585
7 Cock J M, McCormick S (2001). A large family of genes that share homology with CLAVATA3. Plant Physiol , 126(3): 939–942
doi: 10.1104/pp.126.3.939
8 Fiers M, Golemiec E, van der Schors R, van der Geest L, Li K W, Stiekema W J, Liu C M (2006). The CLAVATA3/ESR motif of CLAVATA3 is functionally independent from the nonconserved flanking sequences. Plant Physiol , 141(4): 1284–1292
doi: 10.1104/pp.106.080671
9 Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R, Stiekema W, Liu C M (2005). The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell , 17(9): 2542–2553
doi: 10.1105/tpc.105.034009
10 Fiers M, Ku K L, Liu C M (2007). CLE peptide ligands and their roles in establishing meristems. Curr Opin Plant Biol , 10(1): 39–43
doi: 10.1016/j.pbi.2006.11.003
11 Fletcher J C, Brand U, Running M P, Simon R, Meyerowitz E M (1999). Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science , 283(5409): 1911–1914
doi: 10.1126/science.283.5409.1911
12 Geier F, Lohmann J U, Gerstung M, Maier A T, Timmer J, Fleck C (2008). A quantitative and dynamic model for plant stem cell regulation. PLoS One , 3(10): e3553
doi: 10.1371/journal.pone.0003553
13 Gordon S P, Heisler M G, Reddy G V, Ohno C, Das P, Meyerowitz E M (2007). Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development , 134(19): 3539–3548
doi: 10.1242/dev.010298
14 Gross-Hardt R, Laux T (2003). Stem cell regulation in the shoot meristem. J Cell Sci , 116(Pt 9): 1659–1666
doi: 10.1242/jcs.00406
15 Hass C, Lohrmann J, Albrecht V, Sweere U, Hummel F, Yoo S D, Hwang I, Zhu T, Sch?fer E, Kudla J, Harter K (2004). The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J , 23(16): 3290–3302
doi: 10.1038/sj.emboj.7600337
16 Heisler M G, Ohno C, Das P, Sieber P, Reddy G V, Long J A, Meyerowitz E M (2005). Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol , 15(21): 1899–1911
doi: 10.1016/j.cub.2005.09.052
17 Hobe M, Müller R, Grünewald M, Brand U, Simon R (2003). Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev Genes Evol , 213(8): 371–381
doi: 10.1007/s00427-003-0329-5
18 Hwang I, Sheen J (2001). Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature , 413(6854): 383–389
doi: 10.1038/35096500
19 Jeong S, Trotochaud A E, Clark S E (1999). The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell , 11(10): 1925–1934
20 J?nsson H, Heisler M, Reddy G V, Agrawal V, Gor V, Shapiro B E, Mjolsness E, Meyerowitz E M (2005). Modeling the organization of the WUSCHEL expression domain in the shoot apical meristem. Bioinformatics , 21(Suppl 1): i232–i240
doi: 10.1093/bioinformatics/bti1036
21 Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H, Sakagami Y (2006). A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science , 313(5788): 845–848
doi: 10.1126/science.1128439
22 Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, Sakakibara H, Kyozuka J (2007). Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature , 445(7128): 652–655
doi: 10.1038/nature05504
23 Laux T, Mayer K F, Berger J, Jürgens G (1996). The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development , 122(1): 87–96
24 Leibfried A, To J P, Busch W, Stehling S, Kehle A, Demar M, Kieber J J, Lohmann J U (2005). WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature , 438(7071): 1172–1175
doi: 10.1038/nature04270
25 Lenhard M, Bohnert A, Jürgens G, Laux T (2001). Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell , 105(6): 805–814
26 Lenhard M, Laux T (2003). Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1. Development , 130(14): 3163–3173
doi: 10.1242/dev.00525
27 Leyser H M O, Furner I J (1992). Characterisation of three shoot apical meristem mutants of Arabidopsis thaliana. Development , 116: 397–403
28 Lindsay D L, Sawhney V K, Bonham-Smith P C (2006). Cytokinin-induced changes in CLAVATA1 and WUSCHEL expression temporally coincide with altered floral development in Arabidopsis. Plant Sci , 170: 1111–1117
doi: 10.1016/j.plantsci.2006.01.015
29 Liu C M, Xu Z, Chua N H (1993). Auxin Polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis. Plant Cell , 5(6): 621–630
30 Mayer K F, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998). Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell , 95(6): 805–815
31 Müller B, Sheen J (2008). Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature , 453(7198): 1094–1097
doi: 10.1038/nature06943
32 Müller R, Bleckmann A, Simon R (2008). The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell , 20(4): 934–946
doi: 10.1105/tpc.107.057547
33 Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004). Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell , 16(6):1365–1377
doi: 10.1105/tpc.021477
34 Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008). Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science , 319(5861): 294
doi: 10.1126/science.1150083
35 Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009). A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol , 5(8): 578–580
doi: 10.1038/nchembio.182
36 Philipson W R (1954). Organization of the shoot apex in dicotyledons. Phytomorphogy , 4: 70–75
37 Reinhardt D, Frenz M, Mandel T, Kuhlemeier C (2003). Microsurgical and laser ablation analysis of interactions between the zones and layers of the tomato shoot apical meristem. Development , 130(17): 4073–4083
doi: 10.1242/dev.00596
38 Reinhardt D, Mandel T, Kuhlemeier C (2000). Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell , 12(4): 507–518
39 Riefler M, Novak O, Strnad M, Schmülling T (2006). Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell , 18(1): 40–54
doi: 10.1105/tpc.105.037796
40 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(3): 354–358
doi: 10.1101/gad.252503
41 Sakai H, Aoyama T, Oka A (2000). Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J , 24(6): 703–711
doi: 10.1046/j.1365-313x.2000.00909.x
42 Scheres B (2007). Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol , 8(5): 345–354
doi: 10.1038/nrm2164
43 Schoof H, Lenhard M, Haecker A, Mayer K F X, Jürgens 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(6): 635–644
44 Singh M B, Bhalla P L (2006). Plant stem cells carve their own niche. Trends Plant Sci , 11(5): 241–246
doi: 10.1016/j.tplants.2006.03.004
45 Skoog F, Miller C O (1957). Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol , 54(11): 118–130
46 Steeves T A, Sussex I M (1989). Patterns in plant development. 2nd ed. Cambridge: Cambridge University Press
doi: 10.1017/CBO9780511626227
47 Su Y H, Zhao X Y, Liu Y B, Zhang C L, O’Neill S D, Zhang X S (2009). Auxin-induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. Plant J , 59(3): 448–460
doi: 10.1111/j.1365-313X.2009.03880.x
48 Sussex I M (1955). Morphologenesis in Solanum tuberosum L.: Apical structure and developmental pattern of the juvenile shoot. Phytomorphology , 5: 253–273
49 Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque M P, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K, Jones J D, Taylor C G, Schachtman D P, May S, Sandberg G, Benfey P, Friml J, Kerr I, Beeckman T, Laplaze L, Bennett M J (2008). The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol , 10(8): 946–954
doi: 10.1038/ncb1754
50 To J P, Haberer G, Ferreira F J, Deruère J, Mason M G, Schaller G E, Alonso J M, Ecker J R, Kieber J J (2004). Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell , 16(3): 658–671
doi: 10.1105/tpc.018978
51 Trotochaud A E, Hao T, Wu G, Yang Z, Clark S E (1999). The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell , 11(3): 393–406
52 van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B (1995). Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature , 378(6552): 62–65
doi: 10.1038/378062a0
53 van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997). Short-range control of cell differentiation in the Arabidopsis root meristem. Nature , 390(6657): 287–289
doi: 10.1038/36856
54 Zhu Y F, Wang Y, Li R, Song X, Wang Q, Huang S, Jin J B, Liu C M, Lin J X (2010). Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis. Plant J , 61(2): 223–233
doi: 10.1111/j.1365-313X.2009.04049.x
[1] Dingcheng Gao, Vivek Mittal, Yi Ban, Ana Rita Lourenco, Shira Yomtoubian, Sharrell Lee. Metastatic tumor cells – genotypes and phenotypes[J]. Front. Biol., 2018, 13(4): 277-286.
[2] Tyler Harvey, Chen-Ming Fan. Origin of tendon stem cells in situ[J]. Front. Biol., 2018, 13(4): 263-276.
[3] Syed Baker, Svetlana V. Prudnikova, Tatiana Volova. Siberian plants: untapped repertoire of bioactive endosymbionts[J]. Front. Biol., 2018, 13(3): 157-167.
[4] Thai Q. Dao, Jennifer C. Fletcher. CLE peptide-mediated signaling in shoot and vascular meristem development[J]. Front. Biol., 2017, 12(6): 406-420.
[5] Ian Arthur Palmer, Zhenhua Shang, Zheng Qing Fu. Salicylic acid-mediated plant defense: Recent developments, missing links, and future outlook[J]. Front. Biol., 2017, 12(4): 258-270.
[6] Liang Hu,Edward Trope,Qi-Long Ying. Metabolism of pluripotent stem cells[J]. Front. Biol., 2016, 11(5): 355-365.
[7] Kyle R. Denton,Chongchong Xu,Harsh Shah,Xue-Jun Li. Modeling axonal defects in hereditary spastic paraplegia with human pluripotent stem cells[J]. Front. Biol., 2016, 11(5): 339-354.
[8] Gabrielle Rushing,Rebecca A. Ihrie. Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone[J]. Front. Biol., 2016, 11(4): 261-284.
[9] Paul J. Lucassen,Charlotte A. Oomen. Stress, hippocampal neurogenesis and cognition: functional correlations[J]. Front. Biol., 2016, 11(3): 182-192.
[10] Fatih Semerci,Mirjana Maletic-Savatic. Transgenic mouse models for studying adult neurogenesis[J]. Front. Biol., 2016, 11(3): 151-167.
[11] Jin He. Function of Polycomb repressive complexes in stem cells[J]. Front. Biol., 2016, 11(2): 65-74.
[12] Iftikhar Ali,Nazia Jamil. Polyhydroxyalkanoates: Current applications in the medical field[J]. Front. Biol., 2016, 11(1): 19-27.
[13] Desiree F. Leach,Mitzi Nagarkatti,Prakash Nagarkatti,Taixing Cui. Functional states of resident vascular stem cells and vascular remodeling[J]. Front. Biol., 2015, 10(5): 387-397.
[14] Stuart J. Grice,Ji-Long Liu. A SteMNess perspective of survival motor neuron function: splicing factors in stem cell biology and disease[J]. Front. Biol., 2015, 10(4): 297-309.
[15] James M. Arnold,William T. Choi,Arun Sreekumar,Mirjana Maletić-Savatić. Analytical strategies for studying stem cell metabolism[J]. Front. Biol., 2015, 10(2): 141-153.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed