Molecular and cellular aspects of the shoot apical meristems organization of vascular plants

  • Ekaterina Klimova V. L. Komarov Botanical Institute of the RAS, 2, ul. Professora Popova, St. Petersburg, 197376, Russian Federation; St. Petersburg State University, 7/9, Universitetskaya nab., St. Petersburg, 199034, Russian Federation
  • Olga Voitsekhovskaja V. L. Komarov Botanical Institute of the RAS, 2, ul. Professora Popova, St. Petersburg, 197376, Russian Federation


Transfer of developmental regulators, such as miRNA and transcription factors, through plasmodesmata represents one of the key mechanisms regulating morphogenesis in angiosperms. This mechanism has been termed non-cell-autonomous regulation. At present it is not known whether this process is involved in the morphogenesis of plants belonging to the evolutionarily ancient taxa. Importantly, structure and symplastic organization of apical meristems in the representatives of such taxa significantly differ from those in flowering plants. The non-cell-autonomous transcription factors encoded by the KNOX genes which regulate functions of the shoot apical meristem may become a promising model to study this issue. Refs 102. Figs 3.


shoot apical meristem, plasmodesmata, non-cell-autonomous regulation, transcription factors KNOX


Download data is not yet available.


Ding B., Itaya A., Qi Y. Symplasmic protein and RNA traffic: regulatory points and regulatory factors. Current Opinion in Plant Biology, 2003, vol. 6, pp. 596–602.

Fosket D. Growth and development. Plant physiol., 3rd ed. 2002, pp. 339–374.

Foster T., Lough T., Emerson S., Lee R., Bowman J., Forster R., Lucas W. A surveillance system regulates selective entry of RNA into the shoot apex. Plant Cell., 2002, vol. 14, pp. 1497–1508.

Mezitt L., Lucas W. Plasmodesmal cell-to-cell transport of proteins and nucleic acids. Plant Molec. Biol., 1996, vol. 32, pp. 251–273.

Haywood V., Kragler F., Lucas W. Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell., 2002, pp. 303–325.

Heinlein M. Plasmodesmata: dynamic regulation and role in macromolecular cell-to-cell signaling. Current Opinion in Plant Biology, 2002, vol. 5, pp. 543–552.

Tooke F., Battey N. Models of shoot apical meristem Function. New Phytologist, 2003, vol. 159, pp. 37–52.

Kaplan D., Cooke T. The genius of Wilhelm Hofmeister: the origin of causal-analytical research in plant development. American Journal of Botany, 1996, vol. 84, pp. 1647–1660.

Sinnott E. Plant Morphogenesis. Bot. Science Publications. McGraw-Hill, 1960. 550 p.

Uoring F., Fillips I. Rost rastenii i differentsirovka [Growth and differentiation in plants]. Moscow, Mir Publ., 1984, 512 pp. (In Russian)

Khrzhanovskii V. S. Organografiia i razmnozhenie. Kurs obshchei botaniki [Organography and reproduction. Course of general botany]. Moscow, Vyssh. shk. Publ., 1976, pp. 111–243. (In Russian)

Crockett L. A Study of the Tunica Corpus and Anneau Initial of Irradiated and Normal Stem Apices of Nicotiana tabacum L. Bulletin of the Torrey Botanical Club, vol. 84, pp. 229–236.

Esau K. Plant anatomy; 2nd ed. John Wiley & Sons, New York, USA, 1965. 735 p.

Popham R. Principal types of vegetative shoot apex organization in vascular plants. Ohio J. Sci., 1951, vol. 51, pp. 249–270.

Newman I. Pattern in the meristems of vascular plants. 2. A review of shoot apical meristems of gymnosperms, with comments on apical biology and taxonomy, and a statement of some fundamental concepts. Proc. Linn. Soc., New South Wales, 1961, vol. 86, pp. 9–59.

Gifford E., Foster A. Morphology and evolution of vascular plants. 3rd ed. New York, 1989. 626 p.

Hartel K. Studien an Vegetationspunkten einheimischer Lycopodien. Beitr. Biol. Pfl., 1938, vol. 25, pp. 125–168. (In German)

Philipson W. The significance of apical meristem in the phylogeny of land plants. Plant Systematics and Evolution, 1990, vol. 173, pp. 17–38.

Frank M., Edwards M., Schultz E., McKain M., Fei Z., Sørensen I., Rose J., Scanlon M. Dissecting the olecular signatures of apical cell-type hootmeristems from two ancient land plant lineages. New Phytologist, 2015, pp. 893–904.

Mukherjee K., Brocchieri L. Evolution of plant homeobox genes. eLS.

Burglin T. Analysis of TALE Superclass Homeobox Genes (MEIS, PBC, KNOX, Iroquois, TGIF) Reveals a Novel Domain Conserved between Plants and Animals. Nucleic Acids Res., 1997, vol. 25, pp. 4173–4180.

Ito Y., Nakanomyo I., Motose H., Iwamoto K., Sawa S., Dohmae N., Fukuda H. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science, 2006, vol. 313, pp. 842–845.

Scofield S., Murray J. KNOX Gene Function in Plant Stem Cell Niches. Plant Mol. Biol., 2006, vol. 60, pp. 929–946.

Vollbrecht E., Veit B., Sinha N., Hake S. The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature, 1991, vol. 350, pp. 241–243.

Osipova M. A., Dolgikh E. A., Lutova L. A. Rol' transkriptsionnykh faktorov WOX i KNOX v razvitii rastenii i opukholeobrazovanii [Role of WOX and KNOX transcription factors in plant development and tumor formation]. Ekologicheskaia genetika [Ecological genetics], 2006, vol. IV, issue 4, pp. 3–9. (In Russian)

Sinha N., Williams R., Hake S. Overexpression of the maize homeobox gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Gene Dev., 1993, vol. 7, pp. 787–795.

Smith L., Greene B., Veit B., Hake S. A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development, 1992, vol. 116, pp. 21–30.

Kerstetter R., Vollbrecht E., Lowe B., Veit B., Yamaguchi J., Hake S. Sequence analysis and expression patterns divide the maize Knotted1-like homeobox genes into two classes. Plant Cell, 1994, vol. 6, pp. 1877–1887.

Vollbrecht E., Reiser L., Hake S. Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1. Development, 2000, vol. 127, pp. 3161–3172.

Lee J., Kim D.-M., Lim Y., Pai H.-S. The shooty callus induced by suppression of tobacco CHRK1 receptor-like kinase is a phencopy of the tobacco genetic tumor. Plant Cell Reports, 2004, vol. 23, pp. 397–403.

Lin W.-C. The Arabidopsis LATERAL ORGAN BOUNDARIES–Domain gene ASYMMETRIC LEAVES2 functions in the repression of KNOX gene expression and in adaxial-abaxial patterning. Plant Cell., 2003, vol. 15, pp. 2241–2252.

Chen J., Janssen B., Williams A. A gene fusion at homeobox locus: alterations in leaf shape and implications for morphological evolution. Plant Cell., 1999, vol. 9, pp. 1289–1304.

Bharathan G., Goliber T., Moore C. Homologies in leaf form inferred from KNOXI gene expression during development. Science, 2002, vol. 296, pp. 1858–1860.

Scofield S., Dewitte W., Nieuwland J., Murray J. The Arabidopsis homeobox gene SHOOT MERISTEMLESS has cellular and meristem-organisational roles with differential requirements for cytokinin and CYCD3 activity. The Plant Journal, 2013, vol. 75, pp. 53–66.

Jasinski S., Piazza P., Craft J., Hay A., Woolley L., Rieu I., Phillips A., Hedden P., Tsiantis M. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol., 2005, vol. 15, pp. 1560–1565.

Yanai O., Shani E., Dolezal K., Tarkowski P., Sablowski R., Sandberg G., Samach A., Ori N. Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr. Biol., 2005, vol. 15, pp. 1566–1571.

Frank M., Rupp H., Prinsen E., Motyka V., Van Onckelen H., Schmulling T. Hormone autotrophic growth and differentiation identifies mutant lines of Arabidopsis with altered cytokinin and auxin content or signaling. Plant Physiol., 2000, vol. 122, pp. 721–729.

Frugis G., Giannino D., Mele G., Nicolodi C., Chiappetta A., Bitonti M. B., Innocenti A. M., Dewitte W., Van Onckelen H., Mariotti D. Overexpression of KNAT1 in lettuce shifts leaf determinate growth to a shoot-like indeterminate growth associated with an accumulation of isopentenyl-type cytokinins. Plant Physiol., 2001, vol. 126, pp. 1370–1380.

Rupp H., Frank M., Werner T., Strand M., Schmulling T. Increased steady state mRNA levels of the STM and KNAT1 homeobox genes in cytokinin overproducing Arabidopsis thaliana indicate a role for cytokinins in the shoot apical meristem. The Plant Journal, 1999, vol. 18, pp. 557–563.

Hamant O., Nogue F., Belles-Boix E., Jublot D., Grandjean O., Traas J., Pautot V. The KNAT2 homeodomain protein interacts with ethylene and cytokinin signaling. Plant Physiol., 2001, vol. 130, pp. 657–665.

Reinhardt D., Mandel T., Kuhlemeier C. Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell., 2000, vol. 12, pp. 507–518.

Hooley R. Gibberellins: perception, transduction and responses. Plant Mol. Biol., 1994, vol. 26, pp. 1529–1555.

Hay A., Kaur H., Phillips A., Hedden P., Hake S., Tsiantis M. The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr. Biol., 2002, pp. 1557–1565.

Sakamoto T., Kamiya N., Ueguchi-Tanaka M., Iwahori S., Matsuoka M. KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev., 2001, vol. 15, pp. 581–590.

Bolduc N., Yilmaz A., Mejia-Guerra M., Morohashi K., O’Connor D., Grotewold E., Hake S. Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev., 2012, vol. 26, pp. 1685–1690.

Crawford K., Zambryski P. Plasmodesmata signaling: many roles, sophisticated statutes. Current Opinion in Plant Biol., 1999, vol. 5, pp. 382–387.

Mele G., Ori N., Sato Y., Hake S. The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways. Genes Dev., 2003, vol. 17, pp. 2088–2093.

Groover A., Mansfi eld S., DiFazio S., Dupper G., Fontana J., Millar R. et al. The Populus homeobox gene ARBORKNOX1 reveals overlapping mechanisms regulating the shoot apical meristem and the vascular cambium. Plant Mol. Biol., 2006, vol. 61, pp. 917–932.

Testone G., Condello E., Verde I., Nicolodi C., Caboni E., Dettori M. T. et al. The peach (Prunus persica L. Batsch) genome harbours 10 KNOX genes, which are differentially expressed in stem development, and the class 1 KNOPE1 regulates elongation and lignification during primary growth. J. Exp. Bot., 2012, vol. 63, pp. 5417–5435.

Douglas S., Chuck G., Dengler R., Pelecanda L., Riggs C. KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell., 2002, vol. 14, pp. 547–558.

Douglas S., Riggs C. Pedicel development in Arabidopsis thaliana: contribution of vascular positioning and the role of the BREVIPEDICELLUS and ERECTA genes. Dev. Biol., 2005, vol. 284, pp. 451–463.

Venglat S., Dumonceaux T., Rozwadowski K., Parnell L., Babic V., Keller W. et al. The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 4730–4735.

Townsley B., Sinha N., Kang J. KNOX1 genes regulate lignin deposition and composition in monocots and dicots. Front. Plant Sci., no. 4, 2013, Article 21.

Luquita A., Urli L., Svetaz M. J., Gennaro A. M., Volpintesta R., Palatnik S. et al. Erythrocyte aggregation in rheumatoid arthritis: cell and plasma factor’s role. Clin. Hemorheol. Microcirc., 2009, vol. 41, pp. 49–56.

Palatnik M., Simoes M., Alves Z., Laranjeira N. The 60 and 63 kDa proteolytic peptides of the red cell membrane band-3 protein: their prevalence in human and non-human primates. Hum. Genet., 1990, vol. 86, pp. 126–130.

Rodriguez R., Mecchia M., Debernardi J., Schommer C., Weigel D., Palatnik J. Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development, 2010, vol. 137, pp. 103–112.

Yonekura-Sakakibara K., Tohge T., Matsuda F., Nakabayashi R., Takayama H., Niida R., Watanabe-Takahashi A., Inoue E., Saito K. Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. Plant Cell., 2008, vol. 20, pp. 2160–2176.

Harrison C., Corley S., Moylan E., Alexander D., Scotland R., Langdale J. Independent recruitment of a conserved developmental mechanism during leaf formation. Nature, 2005, vol. 434, pp. 509–514.

Kawai J., Tanabe Y., Soma S., Ito M. Class 1 KNOX gene expression supports the Selaginella rhizophore concept. J. Plant Biol., 2010, vol. 53, pp. 268–274.

Sano R., Jurárez C., Hass B., Sakakibara K., Ito M., Banks J. et al. KNOX homeobox genes potentially have similar function in both diploid unicellular and multicellular meristems, but not haploid meristems. Evolution and Development, 2005, vol. 7, pp. 69–78.

Sundas-Larsson A., Svenson M., Liao H., Engstrom P. A homeobox gene with potential developmental control function in the meristem of the conifer Picea abies. Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 15118–15122.

Hjortswang H., Sundas-Larsson A., Bharathan G., Bozhkov P., von Arnold S., Vahala T. KNOTTED1-like homeobox genes of gymnosperm, Norway spruce, expressed during somatic embryogenesis. Plant Physiol. Biochem., 2002, vol. 40, pp. 837–843.

Ehlers K., Kollmann R. Primary and secondary plasmodesmata: structure, origin and functioning. Protoplasma, 2001, vol. 216, pp. 1–30

Faulkner C., Akman O., Bell K., Jeffree C., Oparka K. Peeking into Pit Fields: A Multiple Twinning Model of Secondary Plasmodesmata Formation in Tobacco. Plant Cell., 2008, vol. 20, pp. 1504–1518.

Walker D., Hill G., Wood S., Smallwood R., Southgate J. Agent-based computational modelling of epithelial cell monolayers: Predicting the effect of exogenous calcium concentrations on the rate of wound closure. Nanobioscience, 2004, vol. 3, pp. 153–163.

Cooke T., Tilney M., Tilney L. Plasmodesmatal networks in apical meristems and mature structures: geometric evidence for both primary and secondary formation of plasmodesmata. BIOS Scientific, 1996, pp. 471–488.

Imaichi R., Hiratsuka R. Evolution of shoot apical meristem structures in vascular plants with respect to plasmodesmatal network. Am. J. Bot., 2007, vol. 94, pp. 1911–1921.

Pryer K., Schuettpelz E., Wolf P., Schneider H., Smith A., Cranfi ll R. Phylogeny and evolution of ferns (Monilophytes) with a focus on the early leptosporangiate divergences. American Journal of Botany, 2004, vol. 91, pp. 582–1598.

Gunning B. E. S., Hughes J. E., Hardham A. R. Formative and proliferative divisions, cell differentiation and developmental changes in the meristem of Azolla roots. Planta, 1978, vol. 143, pp. 121–144.

Ding B., Haudenshield J., Hull R., Wolf S., Beachy R., Lucas W. Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell., 1992, vol. 4, pp. 915–928.

Ding B., Haudenshield J., Willmitzer L., Lucas W. Correlation between arrested secondary plasmodesmal development and onset of accelerated leaf senescence in yeast acid invertase transgenic tobacco plants. Plant J., 1993, vol. 4, pp. 179–189.

Ding B., Lucas W. Secondary plasmodesmata: biogenesis, special functions, and evolution. Membranes: Specialized Functions in Plants. Eds M. Smallwood, P. Knox, D. Bowles. BIOS Scientific Publishers, 1996, pp. 489–506.

Evkaikina A., Romanova M., Voitsekhovskaja O. Evolutionary aspects of non-cell-autonomous regulation in vascular plants: structural background and models to study. Front. Plant. Sci., no. 5:31. 2014.

Kempers R., van Bel A. Symplasmic connections between sieve element and companion cell in the stem phloem of Vicia faba L. have a molecular exclusion limit of at least 10 kDa. Planta, 1997, vol. 201, pp. 195–201.

Oparka K., Cruz S. The great escape: phloem transport and unloading of macromolecules. Plant Physiol. Plant Mol. Biol., 2000, vol. 51, pp. 323–347.

Chen M., Tian G., Gafni Y., Citovsky V. Effects of calreticulin on viral cell-to-cell movement. Plant Physiol., 2005, vol. 138, pp. 1866−1876.

Imlau A., Truernit E., Sauer N. Cell-to-cell and long-distance tracking of green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell., 1999, vol. 11, pp. 309–322.

Deom C., Oliver M., Beachy R. The 30-kilodalton movement protein of tobacco mosaic virus potentiates virus movement. Science, 1987, vol. 237, pp. 389–394.

Waigmann E., Lucas W., Citovsky V., Zambryski P. Direct functional assay for tobacco mosaic virus cell-to-cell movement protein and identification of a domain involved in increasing plasmodesmatal permeability. Proc. Natl. Acad. Sci. USA, 1994, vol. 91, pp. 1433–1437.

Citovsky V., Wong M., Shaw A., Prasad B., Zambryski P. Visualization and characterization of tobacco mosaic virus movement protein binding to singlestranded nucleic acids. Plant Cell, 1992, vol. 4, pp. 397–411.

Tomenius K., Clapham D., Meshi T. Localization by immunogold cytochemistry of the virus-coded 30K protein in plasmodesmata of leaves infected. Virology, 1987, vol. 160, pp. 363–371.

Wolf S., Deom C., Beachy R., Lucas W. Movement protein of tobacco mosaic virus modifies plasmodesmata size exclusion limit. Science, 1989, vol. 246, pp. 377–379.

Jackson D., Veit B., Hake S. Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development, 1994, vol. 120, pp. 405–413.

Lucas W. Plasmodesmata-intercellular channels for macromolecular transport in plants. Curr. Opin. Cell Biol., 1995, pp. 673–680.

Kim J., Yuan Z., Cilia M., Khalfan Z., Jackson D. Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis. Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 4103–4108.

Heinlein M., Epel B. Macromolecular transport and signaling through plasmodesmata. Int. Rev. Cytol., 2004, vol. 235, pp. 93–164.

Xoconostle-Cazares B., Xiang Y., Ruiz-Medrano R., Wang H., Monzer J., Yoo B., McFarland K. C., Franceschi V. R., Lucas W. Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science, 1999, vol. 283, pp. 94–98.

Zavaliev R., Ueki S., Epel B., Citovsky V. Biology of callose (β-1,3-glucan) turnover at plasmodesmata. Protoplasma, 2011, vol. 248, pp. 117–130.

Kragler F., Monzer J., Shash K., Xoconostle-Cazares B., Lucas W. J. Cell-to-cell transport of proteins: Requirement for unfolding and characterization of binding to a putative plasmodesmal receptor. Plant, 1998, vol. 15, pp. 367–381.

Aoki K., Kragler F., Xoconostle-Cázares B., Lucas W. A subclass of plant heat shock cognate 70 chaperones carries a motif that facilitates trafficking through plasmodesmata. Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 16342–16347.

Horwich A., Fenton W., Chapman E., Farr G. Two families of chaperonin: physiology and mechanism. Annu. Rev. Cell Dev. Biol., 2007, vol. 23, pp. 115–145.

Xu X. , Wang J., Xuan Z., Goldshmidt A., Borrill P., Hariharan N., Kim J., Jackson D. Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function. Science, 2011, vol. 333, pp. 1141–1144.

Perbal M.-C., Haughn G., Saedler H., Schwarz-Sommer Z. Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development, 1996, vol. 122, pp. 3433–3441.

Sessions A., Yanofsky M., Weigel D. Cell — cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science, 2000, vol. 289, pp. 779–782.

Helariutta Y., Fukaki H., Wysocka-Diller J., Nakajima K., Jung J., Sena G., Hauser M. T., Benfey P. N. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell, 2000, vol. 101, pp. 555–567.

Nakajima K., Benfey P. Signalling in and out: control of cell division and differentiation in the shoot and root. Plant Cell., 2002, no. 14 (Suppl.), pp. 265–276.

Ruiz-Medrano R., Xoconostle-Cazares B., Lucas W. The phloem as a conduit for inter-organ communication. Current Opinion in Plant Biology, 2001, vol. 4, pp. 202–209.

Wu X., Weigel D., Wigge P. Signaling in plants by intercellular RNA and protein movement. Genes Dev., 2002, vol. 16, pp. 151–158.

Voinnet O., Baulcombe D. Systemic signaling in gene silencing. Nature, 1997, vol. 389, pp. 553.

Voinnet O., Vain P., Angel S., Baulcombe D. Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell, 1998, vol. 95, pp. 177–187.

Vance V., Vaucheret H. RNA silencing in plants — Defense and counterdefense. Science, 2001, vol. 292, pp. 2277–2280.

Mathieu J., Warthmann N., Küttner F., Schmid M. Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr. Biol., 2007, vol. 17, pp. 1055–1060.
How to Cite
Klimova, E., & Voitsekhovskaja, O. (2015). Molecular and cellular aspects of the shoot apical meristems organization of vascular plants. Biological Communications, (4), 18–38. Retrieved from
Full communication