Browse > Article
http://dx.doi.org/10.5010/JPB.2014.41.4.180

Organization and function of shoot apical meristem affecting growth and development in plants  

Lee, Kyu Bae (Department of Biological Science Education, Chosun University)
Publication Information
Journal of Plant Biotechnology / v.41, no.4, 2014 , pp. 180-193 More about this Journal
Abstract
In plants, a shoot apex has a small region known as the shoot apical meristem (SAM) having a group of dividing (initiating) cells. The SAM gives rise to all the groundabove structures of plants throughout their lifetime, and thus it plays important role in growth and development of plants. This review describes theories to explain the SAM organization and function developed over the last 250 years. Since in 1759 German botanist C. F. Wolff has described firstly the SAM, in 1858 Swiss botanist C. N${\ddot{a}}$geli proposed the apical cell theory from the observation of a large single apical cell in the SAM of seedless vascular plants: however, this view was recognized to be unsuitable to seed plants. In 1868, German botanist J. Hanstein suggested the histogen theory: this concept subdividing the SAM into dermatogen, periblem, and plerome was unable to generally apply to seed plants. In 1924, German botanist A. Schmidt proposed the tunica-corpus theory from the examination of angiosperm SAM in which two parts show different planes of cell division: this theory was proved to be not suitable to gymnosperm SAM, not have stable surface tunica layer. In 1938, American botanist A. Foster described zones in gymnosperm SAM based on the cytohistologic differentiation and thus called it a cytohistological zonation theory. With works by E. Gifford, in 1954, this zonation pattern was demonstrated to be also applicable to angiosperm SAM. As another theory, in 1952 French botanist R. Buvat proposed the m${\acute{e}}$rist${\grave{e}}$me d'attente (waiting meristem) theory: however, this concept was confuted because of its negation of function during vegetative growth phase to central initial cells. Rescent studies with Arabidopsis thaliana have found that formation and maintenance of the SAM are under the control of selected genes: SHOOTMERISTEMLESS (STM) gene forms the SAM, and WUSCHEL (WUS) and CLAVATA (CLV) genes function in maintaining the SAM; signaling between WUS and CLV genes act through a negative feedback loop.
Keywords
Apical cell; Arabidopsis; Cytohistological zonation; Histogen; M${\acute{e}}$rist${\grave{e}}$me d'attente (waiting meristem); Shoot apical meristem; Tunica-corpus;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Lenhard M, Bohnert A, Jurgens G, Laux T (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105: 805-814   DOI   ScienceOn
2 Lenhard M, Jurgens G, Laux T (2002) The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation. Development 129:3195-3206
3 Leyser O, Day S (2003) Mechanism in plant development. Blackwell Publishing
4 Li Y, Zheng L, Corke F, Smith C, Bevan MW (2008) Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev 22:1331-1336   DOI
5 Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793-803   DOI   ScienceOn
6 Long JA, Barton MK (1998) The development of apical embryonic pattern in Arabidopsis. Development 125:3027-3055
7 Long JA, Barton MK (2000) Initiation of axillary and floral meristems in Arabidopsis. Dev Biol 218:341-353   DOI
8 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   DOI   ScienceOn
9 Lyndon RF (1970) Rate of cell division in the shoot apical meristem of Pisum. Ann Bot (London) 34:1-17   DOI
10 Lyndon RF (1976) The shoot apex. In: Yeoman MM (ed), Cell Division in Higher Plants. Academic Press, New York. pp 285-314
11 Lyndon RF (1998) The shoot apical meristem, its growth and development. Cambridge University Press. Cambridge.
12 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
13 Mauseth JD (1978) An investigation of the morphogenetic mechanisms which control the development of zonation in seedling shoot apical meristems. Am J Bot 65:158-167   DOI
14 Mauseth JD (1988) Plant Anatomy. The Benjamin/Cummings Publishing Co., Inc., Menlo Park, California, p 88
15 Mayer KFX, 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   DOI   ScienceOn
16 Medford JI (1992) Vegetative apical meristems. Plant Cell 4: 1029-1039   DOI
17 Medford JI, Behringer FJ, Callos JD, Feldmann KA (1992) Normal and abnormal development in the Arabidopsis vegetative shoot apex. Plant Cell 4:631-643   DOI
18 Meinke DW, Cherry JM, Dean C, Rounsley SD, Koornneef M (1998) Arabidopsis thaliana: A Model Plant for Genome Analysis. Science 282:62-682
19 Meyerowitz EM (1997) Genetic control of cell division patterns in developing plants. Cell 88:299-308   DOI
20 Meyerowitz EM (2001) Prehistory and History of Arabidopsis Research. Plant Physiol 125:15-19   DOI
21 Miwa H, Kinoshita A, Fukuda H, Sawa S (2009) Plant meristems: CLAVATA3/ ESR-related signalling in the shoot apical meristem and the root apical meristem. J Plant Res 122:31-39   DOI
22 Nilsson O, Lee I, Blazquez MA, Weigel D (1998) Flowering-time genes modulate the response to LEAFY activity. Genetics 150:403-410
23 Moore R, Clark WD, Vodopich D (1998) Botany. 2nd ed. WBC McGraw-Hill
24 Murray AH, Jones A, Godin C, Traas J (2012) Systems analysis of shoot apical meristem growth and development: Integrating hormonal and mechanical signaling. Plant Cell 24:3907-3919   DOI
25 Nageli C (1858) Das Wachsthum des Stammes und der Wurzel bei den Gefasspflanzen und die Anordnung der Gefasstrange in Stengel. Beitr Wissenschaft Bot 1:1-156
26 Page DR, Grossniklaus U (2002) The art and design of genetic screens : Arabidopsis thaliana. Nat Rev Genet 3:124-136   DOI
27 Pilkington M (1929) The regeneration of the stem apex. New Phytol 28:37-53   DOI
28 Poethig RS, Sussex IM (1985) The developmental morphology and growth dynamics of the tobacco leaf. Planta 165:158-169   DOI
29 Popham RA, Chan AP (1950) Zonation in the vegetavive stem tip of Chrysanthemum morifolium Bailey. Am J Bot 37:476-484   DOI
30 Reddy GV (2008) Live-imaging stem-cell homeostasis in the Arabidopsis shoot apex. Curr Opin Plant Biol 11:88-93   DOI
31 Reddy GV, Meyerowitz EM (2005) Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apex. Science 310:663-667   DOI
32 Reddy GV, Heisler MG, Ehrhardt DW, Meyerowitz EM (2004) Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development 131:4225-4237   DOI   ScienceOn
33 Schmidt A (1924) Histologische Studien an Phanerogamen Vegetationspunkten. Botanik Archiv 8:345-404
34 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 130:4073-4083   DOI   ScienceOn
35 Saint-Come R (1966) Applications des techniques histoautogadiographiques et des methods a l'etude du functionnement apical chez le Coleus blumei Beneth. Rev Gen Bot 73:241-324
36 Sekhar KNC, Sawhney VK (1985) Ultrastructure of the shoot apex of tomato (Solanum lycopersicum). Am J Bot 72:1813-1822   DOI
37 Schoof H, Lenhard M, Haecker A, Mayer KFX, Jurgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635-644   DOI   ScienceOn
38 Scofield S, Murray JAH (2006) KNOX gene function in plant stem cell niches. Plant Mol Biol 60:929-946   DOI
39 Sinha N (1999) Leaf development in angiosperms. Annu Rev Plant Physiol Plant Mol Biol 50:419-446   DOI   ScienceOn
40 Smith LG, Greene B, Veit, Hake S (1992) A dominant mutation in the maize homeobox gene, Knotted-1, causes itsectopic expression in leaf cells with altered fates. Development 116:21-30
41 Snow M, Snow R (1951) Minimum areas and leaf determination. Philos Trans R Soc Lond Ser B 139:545-566
42 Steeves TA (2006) The shoot apical meristem: an historical perspective. Can J Bot 84: 1629-1633   DOI
43 Sussex IM (1964) The permanence of meristems: Developmental organizers or reactors to exogenous stimuli? Brookhaven Symp Biol 16:1-12
44 Steeves TA, Sussex IM (1989) Patterns in plant development. 2nd ed. Cambridge University Press, Cambridge, UK
45 Stewart RN, Dermen H (1970) Determination of number and mitotic activity of shoot apical initial cells by analysis of mericlinal chimeras. Am J Bot 57:816-826   DOI
46 Sussex IM (1952) Regeneration of the potato shoot apex. Nature 170:755-757
47 Takacs EM, Li J, Du C, Ponnala L, Janick-Buckner D, Yu J, Muehlbauer GJ, Schnable PS, Timmermans MCP, Sun Q, Nettleton D, Scanlon MJ (2010) Ontogeny of the maize shoot apical meristem. Plant Cell 24:3219-3234
48 The Arabidopsis Genome Initiative (2001) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815
49 Tooke F, Battey N (2003) Models of shoot apical meristem function. New Phytol 159:37-52   DOI
50 Turck F, Fornara F, Coupland G, 2008. Regulation and identity of florigen, FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573-594   DOI   ScienceOn
51 van Lijsebettens M, Clarke J (1998) Leaf development in Arabidopsis. Plant Physiol Biochem 36:47-60   DOI
52 Vaughn JG (1952) Structure of the angiosperm apex. Nature 169:458-459   DOI
53 Vaughn JG (1955) The morphology and growth of the vegetative and reproductive apices of Arabidopsis thaliana (L) Heynh, Capsella bursapastoris (L) Medic and Anagellis arrensis. J Linn Soc Bot 55:279-30 x 240   DOI
54 Weigel D, Jurgens G (2002) Stem cells that make stems. Nature 415:751-754   DOI   ScienceOn
55 Vernoux T, Autran D, Trass J (2000) Developmental control of cell divison patterns in the shoot apex. Plant Mol Biol 43:569-581   DOI
56 Vernoux T, Besnard F, Trass J (2010) Auxin at the shoot apical meristem. Cold Spring Harb Symp Quant Biol 2 a001487
57 Wardlaw CW (1957) On the organization and reactivity of the shoot apex in vascular plants. Am J Bot 44:176-185   DOI
58 Williams L, Fletcher JC (2005) Stem cell regulation in the Arabidopsis shoot apical meristem. Curr Opin Plant Biol 8:582-586   DOI   ScienceOn
59 Wolff CF (1759) Theoria Generationis. Verlag von Wielhelm Engelman, Leipzig, Germany
60 Yadav RK, Girke T, Pasala S, Xie M, Reddy GV (2009) Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc Nat Acad Sci 106:494
61 Barton MK, Poethig RS (1993) Formation of the shoot apical meristem in Arabidopsis thaliana: An analysis of development in the wild type and in the shoot meristemless mutant. Development 1119:823-831
62 Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana. Sceince 301:653-656   DOI
63 Anastasiou E, Lenhard M (2007) Growing up to one's standard. Cur Opi Plant Biol 10:63-69   DOI
64 Barton MK (2010) Twenty years on: The inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol 341:95-113   DOI
65 Beck C (2005) An Introduction to Plant Structure and Development. Cambridge University Press, Cambridge, p 86
66 Bierhorst DW (1971) Morphology of vascular plants. Macmillian, New York
67 Bierhorst DW (1977) On the stem apex, leaf initiation and early leaf ontogeny in filicalean fern. Am J Bot 64:125-152   DOI
68 Bowman JL, Floyd SK (2008) Patterning and polarity in seed plant shoots. Annual Rev Plant Biol 59:67-88   DOI
69 Bosca S, Knauer S, Laux T (2011) Embryonic development in Arabidopsis thaliana: from the zygote division to the shoot meristem. Front Plant Sci 2:1-6
70 Bowman J (1994) Arabidopsis, An Atlas of Morphology and Development. Springer Verlag, New York
71 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   DOI   ScienceOn
72 Brooks L III, Strable J, Zhang X, Ohtsu K, Zhou R, Sarkar A, Hargreaves S, Elshire1 RJ, Eudy D, Pawlowska T, Ware D, Janick-Buckner D, Buckner B, Timmermans MCP, Schnable PS, Nettleton D, Scanlon MJ (2009) Microdissection of shoot meristem functional domains. PLoS Genetics 5(5) e1000476   DOI
73 Brown WV, Heimsch C, Emery HP (1957) The organization of the grass shoot apex and systematics. Am J Bot 444:590-595
74 Brutnell TP, Langdale JA (1998) Signals in leaf development. Adv Bot Res 28:161-195   DOI
75 Buvat R (1952) Structure, evolution et fonctionnement du meristeme apical de quelques dicotyledones. Ann Sci Nat Bot Biol 13:199-300
76 Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Martienssen RA (2000) Asymmetric leaves1mediates leaf patterning and stem cell function in Arabidopsis. Nature 408: 967-971   DOI   ScienceOn
77 Carles CC, Fletcher JC (2003) Shoot apical meristem maintenance: the art of a dynamic balance. Trends Plant Sci 8:394-401   DOI   ScienceOn
78 Clowes FAL (1959) Adenin incorporation and cell division in shoot apices. New phytol 58:16-19   DOI
79 Clark SE (2001) Cell signalling at the shoot meristem. Nature Rev Mol Cell Biol 2:276-284   DOI   ScienceOn
80 Clark SE, Running MP, Meyerowitz EM (1995) CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121:2057-2067
81 Conti L, Bradley D (2007) TERMINAL FLOWER1 is a mobile signal controlling Arabidopsis architecture. Plant Cell 19:767-778   DOI   ScienceOn
82 Corson GE Jr, Gifford EM Jr (1969) Histochemical studies of the shoot apex of Datura stramonium during transition to flowering. Phytomorphology 19:189-196
83 Cutter EG (1959) On the theory of phyllotaxis and histogenesis. Biol Rev 34:243-263
84 Cutter EG (1980) Plant anatomy: Experimental and interpretation. Part 2 Organs. Edward Arnold. p 56
85 Davis EL, Rennie P, Steeves TA (1979) Further analytical and experimental studies on the shoot apex of Helianthus annuus: variable activity in the central zone. Can J Bot 57:971-980   DOI
86 Dinneny JR, Yadegari R, Fischer RL, Yanofsky MF, Weigel D (2004) The role of JAGGED in shaping lateral organs. Development 131:1101-1110   DOI
87 Dodsworth S (2009) A diverse and intricate signalling network regulates stem cell fate in the shoot apical meristem. Dev Biol 336:1-9   DOI
88 Evert RF (2006) Esau's plant anatomy. Meristems, cells, tissues of the plant body-Their structure, function, and development. John Wiley & Sons, Inc, Publication
89 Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T (1996) The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10:967-979   DOI
90 Esau K (1977) Anatomy of seed plants. 2nd ed. Wiley, New York
91 Fahn A (1990) Plant Anatomy. 4th ed. Butterworth-Heinemann, Oxford, p 61
92 Fletcher JC, Meyerowitz EM (2000) Cell signalling within the shoot meristem. Curr Opin Plant Biol 3:23-30   DOI
93 Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signalling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911-1914   DOI
94 Foster AS (1938) Structure and growth of the shoot apex in Gingko biloba. B Torrey Bot Club 65:531-556   DOI
95 Foster AS (1939) Problems of structure, growth and evolution in the shoot apex of seed plants. Bot Rev 5:454-470   DOI
96 Foster AS (1943) Zonal structure and growth of the shoot apex in Microcycas calocoma (Miq.) A. DC. Am J Bot 30:56-73   DOI
97 Gallois J, Woodward C, Reddy GV, Sablowski R (2002) Combined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic organogenesis in Arabidopsis. Development 129:3207-3217
98 Gifford EM Jr, Corson GE Jr (1971) The shoot apex in seed plants. Bot Rev 37:143-229   DOI
99 Gifford EM Jr (1950) The structure and development of the shoot apex in certain woody Ranales. Am J Bot 37:595-611   DOI
100 Gifford EM Jr (1954) The shoot apex in angiosperms. Bot Rev 20:477-529   DOI
101 Gifford EM Jr, Kupila S, Yamaguchi S (1963) Experiments in the application of H3-thymidine and adenine-8-C14 to shoot tips. Phytomorphology 13:14-22
102 Gifford EM Jr, Polito VS, Nitayangkura S (1979) The epical cell in shoot and roots of certain fern: A reevaluation of its functional role in histogenesis. Plant Sci Lett 15:305-311   DOI
103 Gross-Hardt R, Laux T (2003) Stem cell regulation in the shoot meristem. J Cell Sci 116:1659-1666   DOI   ScienceOn
104 Haecker A, Laux E (2001) Cell-cell signaling in the shoot meristem. Curr Opin Plant Biol 4:441-446   DOI
105 Hall LN, Langdale JA (1996) Molecular genetics of cellular differentiation in leaves. New Phytol 132:533-553   DOI
106 Hanstein J (1868) Die Sheitzellgruppe in Vegetationspunkt der Phanerogamen. In: Festschr Friedrich Wilhelms Universtat Bonn. Niederrhein Ges Natur und Heilkunde, Marcus, Bonn, pp 109-134
107 Hu YX, Xie O, Chua NH (2003) The Arabidopsis auxininducible gene ARGOS controls lateral organ size. Plant Cell 15:1951-1961   DOI   ScienceOn
108 Irish VF, Sussex IM (1992) A fate map of the Arabidopsis embryonic shoot apical meristem. Development 115:745-753
109 Kayes JM, Clark SE (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125: 3842-2851
110 Johnson MA (1951) The shoot apex in gymnosperms. Phytomorphology 1:188-204
111 Kessler S, Townsley B, Sinha N (2006) L1 division and differentiation patterns influence shoot apical meristem maintenance. Plant Physiol 141:1349-1362   DOI
112 Kurth E (1981) Mitotic activity in the root apex of the water fern Marsilea vestia Hook. And Grev. Am J Bot 68:881-896   DOI
113 Kwiatkowska D (2008) Flowering and apical meristem growth dynamics. J Exp Bot 59:187-201   DOI
114 Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WN, Ploetz L, Singh S, Wensel A, Eva Huala (2011) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40:D1202-D1210
115 Laufs P, Grandjean O, Jonak C, Kieu K, Traas J (1998) Cellular parameters of the shoot apical meristem in Arabidopsis. Plant Cell 10:1375-1389   DOI
116 Laux T, Mayer KFX, Berger J, Jurgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87-96
117 Lee KB (2012) Plant Morphology. 2nd ed, Life Science Publishing Co. Seoul, pp 49-51
118 Lenhard M, Laux T (1999) Shoot meristem formation and maintenance. Curr Opin Plant Biol 2:44-50   DOI