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Russian Journal of Plant Physiology

, Volume 61, Issue 5, pp 571–589 | Cite as

Lateral meristems of higher plants: Phytohormonal and genetic control

  • I. E. Dodueva
  • M. S. Gancheva
  • M. A. Osipova
  • V. E. Tvorogova
  • L. A. Lutova
Reviews

Abstract

Lateral meristems (pericycle, procambium and cambium, phellogen) are positioned in parallel to the lateral surface of the organ, where they are present, and produce concentric layers of undifferentiated cells. Primary lateral meristems, procambium and pericycle, arise during embryogenesis; secondary lateral meristems, cambium and phellogen, — during post embryonic development. Pericycle is most pluripotent plant meristem, as it may give rise to a variety of other types of meristems: lateral meristems (cambium, phellogen), apical meristems of lateral roots, and also shoot meristems during plant in vitro regeneration. Procambium and cambium developing from it give rise to the vascular tissues of the stems and roots, ensuring their thickening. The review considers the genetic control of lateral meristem development and the role of phytohormones in the control of their activities.

Keywords

higher plants meristems pericycle cambium lateral roots regeneration vascular system secondary growth cytokinins auxins CLE peptides transcription factors 

Abbreviations

AM

apical meristem

CK

cytokinins

LM

lateral meristem

LR

lateral root

NPA

naphtylphthalamic acid

RAM

root apical meristem

SAM

shoot apical meristem

TF

transcription factor

VS

vascular system

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References

  1. 1.
    Pautov, A.A., Morfologiya i anatomiya vegetativnykh organov rastenii, (Morphology and Anatomy of Plant Vegetative Organs), St. Petersburg: St. Petersburg Gos. Univ., 2012.Google Scholar
  2. 2.
    Scheres, B., Wolkenfelt, H., Willemsen, V., Terlouw, M., Lawson, E., Dean, C., and Weisbeek, P., Embryonic origin of the Arabidopsis primary root and root meristem initials, Development, 1994, vol. 120, pp. 2475–2487.Google Scholar
  3. 3.
    Su, Y.H., Liu, Y.B., and Zhang, X.S., Auxin-cytokinin interaction regulates meristem development, Mol. Plant, 2011, vol. 4, pp. 616–625.PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Bishopp, A., Help, H., El-Showk, S., Weijers, D., Scheres, B., Friml, J., Benková, E., Mähönen, A.P., and Helariutta, Y., A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots, Curr. Biol., 2011, vol. 21, pp. 917–926.PubMedCrossRefGoogle Scholar
  5. 5.
    Dodueva, I.E., Yurlova, E.V., Osipova, M.A., and Lutova, L.A., CLE peptides are universal regulators of meristem development, Russ. J. Plant Physiol., 2012, vol. 59, pp. 14–27.Google Scholar
  6. 6.
    Burglin, T., Analysis of TALE superclass homeobox genes (MEINOX, PBS, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plant and animals, Nucleic Acids Res., 1997, vol. 25, pp. 4173–4180.PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Jasinski, S., Piazza, P., Craft, J., Hay, A., Woolley, L., Rieu, I., Phillips, A., Hedden, P., and Tsiantis, M., KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities, Curr. Biol., 2005, vol. 6, pp. 1560–1565.CrossRefGoogle Scholar
  8. 8.
    Leibfried, A., To, J.P., Busch, W., Stehling, S., Kehle, A., Demar, M., Kieber, J.J., and Lohmann, J.U., WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators, Nature, 2005, vol. 438, pp. 1172–1175.PubMedCrossRefGoogle Scholar
  9. 9.
    Long, J.A., Moan, E.I., Medford, J.J., and Barton, M.K., A member of the KNOTTED class of homeodomain proteins encoded by the SHOOTMERISTEMLESS gene of Arabidopsis, Nature, 1996, vol. 379, pp. 66–69.PubMedCrossRefGoogle Scholar
  10. 10.
    Truernit, E., Siemering, K.R., Hodge, S., Grbic, V., and Haseloff, J., A map of KNAT gene expression in the Arabidopsis root, Plant Mol. Biol., 2006, vol. 60, pp. 1–20.PubMedCrossRefGoogle Scholar
  11. 11.
    Frugis, G., Giannino, D., Mele, G., Nicolodi, C., Chiappetta, A., Bitonti, M.B., Innocenti, A.M., Dewitte, W., van Onckelen, H., and 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.PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Rupp, H.M., Frank, M., Werner, T., Strnad, M., and Schmülling, 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, Plant J., 1999, vol. 18, pp. 557–563.PubMedCrossRefGoogle Scholar
  13. 13.
    Testone, G., Condello, E., Verde, I., Nicolodi, C., Caboni, E., Dettori, M.T., Vendramin, E., Bruno, L., Bitonti, M.B., Mele, G., and Giannino, D., The peach (Prunus persica L. Batsch) genome harbors 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.PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Hay, A., Barkoulas, M., and Tsiantis, M., ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in arabidopsis, Development, 2006, vol. 133, pp. 3955–3961.PubMedCrossRefGoogle Scholar
  15. 15.
    Guo, M., Thomas, J., Collins, G., and Timmermans, M.C., Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis, Plant Cell, 2008, vol. 20, pp. 48–58.PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Stahl, Y. and Simon, R., Plant primary meristems: shared functions and regulatory mechanisms, Curr. Opin. Plant Biol., 2010, vol. 13, pp. 53–58.PubMedCrossRefGoogle Scholar
  17. 17.
    Ji, J., Strable, J., Shimizu, R., Koenig, D., Sinha, N., and Scanlon, M.J., WOX4 promotes procambial development, Plant Physiol., 2010, vol. 152, pp. 1346–1356.PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F., Jürgens, G., and Laux, T., The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes, Cell, 2000, vol. 100, pp. 635–644.PubMedCrossRefGoogle Scholar
  19. 19.
    Ito, Y., Nakanomyo, I., Motose, H., Iwamoto, K., Sawa, S., Dohmae, N., and Fukuda, H., Dodeca-CLE peptides as suppressors of plant stem cell differentiation, Science, 2006, vol. 313, pp. 842–845.PubMedCrossRefGoogle Scholar
  20. 20.
    Whitford, R., Fernandez, A., de Groodt, R., Ortega, E., and Hilson, P., Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 18 625–18 630.CrossRefGoogle Scholar
  21. 21.
    Stahl, Y. and Simon, R., Is the Arabidopsis root niche protected by sequestration of the CLE40 signal by its putative receptor ACR4? Plant Signal. Behav., 2009, vol. 4, pp. 634–635.PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Hirakawa, Y., Kondo, Y., and Fukuda, H., TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis, Plant Cell, 2010, vol. 22, pp. 2618–2629.PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Burssens, S., de Almeida, E.J., Beeckman, T., Richard, C., Shaul, O., Ferreira, P., van Montagu, M., and Inzé, D., Developmental expression of the Arabidopsis thaliana CycA2;1 gene, Planta, 2000, vol. 211, pp. 623–631.PubMedCrossRefGoogle Scholar
  24. 24.
    De Smet, I., Vanneste, S., Inzé, D., and Beeckman, T., Lateral root initiation or the birth of a new meristem, Plant Mol. Biol., 2006, vol. 60, pp. 871–887.PubMedCrossRefGoogle Scholar
  25. 25.
    Ferguson, B.J., Indrasumunar, A., Hayashi, S., Lin, M.H., Lin, Y.H., Reid, D.E., and Gresshoff, P.M., Molecular analysis of legume nodule development and autoregulation, J. Integr. Plant Biol., 2010, vol. 52, pp. 61–76.PubMedCrossRefGoogle Scholar
  26. 26.
    Baum, S.F., Dubrovsky, J.G., and Rost, T.L., Apical organization and maturation of the cortex and vascular cylinder in Arabidopsis thaliana (Brassicaceae) roots, Am. J. Bot., 2002, vol. 89, pp. 908–920.PubMedCrossRefGoogle Scholar
  27. 27.
    Atta, R., Laurens, L., Boucheron-Dubuisson, E., Guivarc-h, A., Carnero, E., Giraudat-Pautot, V., Rech, P., and Chriqui, D., Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro, Plant J., 2009, vol. 57, pp. 626–644.PubMedCrossRefGoogle Scholar
  28. 28.
    Parizot, B., Laplaze, L., Ricaud, L., Boucheron-Dubuisson, E., Bayle, V., Bonke, M., de Smet, I., Poethig, S.R., Helariutta, Y., Haseloff, J., Chriqui, D., Beeckman, T., and Nussaume, L., Diarch symmetry of the vascular bundle in Arabidopsis root encompasses the pericycle and is reflected in distich lateral root initiation, Plant Physiol., 2008, vol. 146, pp. 140–148.PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Mähönen, A.P., Higuchi, M., Törmäkangas, K., Miyawaki, K., Pischke, M.S., Sussman, M.R., Helariutta, Y., and Kakimoto, T., Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis, Curr. Biol., 2006, vol. 16, pp. 1116–1122.PubMedCrossRefGoogle Scholar
  30. 30.
    Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R., and Jurgens, G., Effluxdependent auxin gradients establish the apical-basal axis of Arabidopsis, Nature, 2003, vol. 426, pp. 147–153.PubMedCrossRefGoogle Scholar
  31. 31.
    Parizot, B., Roberts, I., Raes, J., Beeckman, T., and de Smet, I., In silico analyses of pericycle cell populations reinforce their relation with associated vasculature in Arabidopsis, Phil. Trans. R. Soc. Lond. B: Biol. Sci., 2012, vol. 367, pp. 1479–1488.CrossRefGoogle Scholar
  32. 32.
    Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K., Jung, J., Sena, G., Hauser, M.T., and Benfey, P.N., The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling, Cell, 2000, vol. 101, pp. 555–567.PubMedCrossRefGoogle Scholar
  33. 33.
    Di Laurenzio, L., Wysocka-Diller, J., Malamy, J.E., Pysh, L., Helariutta, Y., Freshour, G., Hahn, M.G., Feldmann, K.A., and Benfey, P.N., The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root, Cell, 1996, vol. 86, pp. 423–433.PubMedCrossRefGoogle Scholar
  34. 34.
    Cui, H., Hao, Y., Kovtun, M., Stolc, V., Deng, X.W., Sakakibara, H., and Kojima, M., Genome-wide direct target analysis reveals a role for SHORT-ROOT in root vascular patterning through cytokinin homeostasis, Plant Physiol., 2011, vol. 157, pp. 1221–1231.PubMedCentralPubMedCrossRefGoogle Scholar
  35. 35.
    Carlsbecker, A., Lee, J.Y., Roberts, C.J., Dettmer, J., Lehesranta, S., Zhou, J., Lindgren, O., MorenoRisueno, M.A., Vaten, A., and Thitamadee, S., Cell signalling by microRNA165/6 directs gene dosedependent root cell fate, Nature, 2010, vol. 465, pp. 316–321.PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Emery, J.F., Floyd, S.K., Alvarez, J., Eshed, Y., Hawker, N.P., Izhaki, A., Baum, S.F., and Bowman, J.L., Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes, Curr. Biol., 2003, vol. 13, pp. 1768–1774.PubMedCrossRefGoogle Scholar
  37. 37.
    Okushima, Y., Mitina, I., Quach, H.L., and Theologis, A., AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator, Plant J., 2005, vol. 43, pp. 29–46.PubMedCrossRefGoogle Scholar
  38. 38.
    Dubrovsky, J.G., Doerner, P.W., Colón-Carmona, A., and Rost, T.L., Pericycle cell proliferation and lateral root initiation in Arabidopsis, Plant Physiol., 2000, vol. 124, pp. 1648–1657.PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Demchenko, N.P. and Demchenko, K.N., Resumption of DNA synthesis and cell division in wheat roots as related to lateral root initiation, Russ. J. Plant Physiol., 2001, vol. 48, pp. 755–763.Google Scholar
  40. 40.
    Jansen, L., Roberts, I., de Rycke, R., and Beeckman, T., Phloem-associated auxin response maxima determine radial positioning of lateral roots in maize, Phil. Trans. R. Soc. Lond. B: Biol. Sci., 2012, vol. 367, pp. 1525–1533.CrossRefGoogle Scholar
  41. 41.
    Beeckman, T., Burssens, S., and Inzé, D., The pericell-cycle in Arabidopsis, J. Exp. Bot., 2001, vol. 52, pp. 403–411.PubMedCrossRefGoogle Scholar
  42. 42.
    Roudier, F., Fedorova, E., Lebris, M., Lecomte, P., Gyorgyey, J., Vaubert, D., Horvath, G., Abad, P., Kondorosi, A., and Kondorosi, E., The Medicago species A2-type cyclin is auxin regulated and involved in meristem formation but dispensable for endoreduplicationassociated developmental programs, Plant Physiol., 2003, vol. 131, pp. 1091–1103.PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Dubrovsky, J.G., Sauer, M., Napsucialy-Mendivil, S., Ivanchenko, M.G., Friml, J., Shishkova, S., Celenza, J., and Benková, E., Auxin acts as a local morphogenetic trigger to specify lateral root founder cells, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 8790–8794.PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Benková, E. and Bielach, A., Lateral root organogenesis — from cell to organ, Curr. Opin. Plant Biol., 2010, vol. 13, pp. 677–683.PubMedCrossRefGoogle Scholar
  45. 45.
    Ditengou, F.A., Teale, W.D., Kochersperger, P., Flittner, K.A., Kneuper, I., van der Graaff, E., Nziengui, H., Pinosa, F., Li, X., Nitschke, R., Laux, T., and Palme, K., Mechanical induction of lateral root initiation in Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 18 818–18 823.CrossRefGoogle Scholar
  46. 46.
    De Rybel, B., Vassileva, V., Parizot, B., Demeulenaere, M., Grunewald, W., Audenaert, D., van Campenhout, J., Overvoorde, P., Jansen, L., Vanneste, S., Möller, B., Wilson, M., Holman, T., van Isterdael, G., Brunoud, G., Vuylsteke, M., Vernoux, T., de Veylder, L., Inzé, D., Weijers, D., Bennett, M.J., and Beeckman, T., A novel Aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity, Curr. Biol., 2010, vol. 20, pp. 1697–1706.PubMedCrossRefGoogle Scholar
  47. 47.
    Laplaze, L., Benková, E., Casimiro, I., Maes, L., Vanneste, S., Swarup, R., Weijers, D., Calvo, V., Parizot, B., Herrera-Rodriguez, M.B., Offringa, R., Graham, N., Doumas, P., Friml, J., Bogusz, D., Beeckman, T., and Bennett, M., Cytokinins act directly on lateral root founder cells to inhibit root initiation, Plant Cell, 2007, vol. 19, pp. 3889–3900.PubMedCentralPubMedCrossRefGoogle Scholar
  48. 48.
    Ruzicka, K., Simásková, M., Duclercq, J., Petrásek, J., Zazímalová, E., Simon, S., Friml, J., van Montagu, M.C., and Benková, E., Cytokinin regulates root meristem activity via modulation of the polar auxin transport, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 4284–4299.PubMedCentralPubMedCrossRefGoogle Scholar
  49. 49.
    Bielach, A., Podlesáková, K., Marhavy, P., Duclercq, J., Cuesta, C., Müller, B., Grunewald, W., Tarkowski, P., and Benková, E., Spatiotemporal regulation of lateral root organogenesis in Arabidopsis by cytokinin, Plant Cell, 2012, vol. 24, pp. 3967–3981.PubMedCentralPubMedCrossRefGoogle Scholar
  50. 50.
    Chang, L., Ramireddy, E., and Schmülling, T., Lateral root formation and growth of Arabidopsis is redundantly regulated by cytokinin metabolism and signalling genes, J. Exp. Bot., 2013, vol. 64, pp. 5021–5032.PubMedCentralPubMedCrossRefGoogle Scholar
  51. 51.
    DiDonato, R.J., Arbuckle, E., Buker, S., Sheets, J., Tobar, J., Totong, R., Grisafi, P., Fink, G.R., and Celenza, J.L., Arabidopsis ALF4 encodes a nuclearlocalized protein required for lateral root formation, Plant J., 2004, vol. 37, pp. 340–353.PubMedCrossRefGoogle Scholar
  52. 52.
    Sarkar, A.K., Luijten, M., Miyashima, S., Lenhard, M., Hashimoto, T., Nakajima, K., Scheres, B., Heidstra, R., and Laux, T., Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers, Nature, 2007, vol. 446, pp. 811–814.PubMedCrossRefGoogle Scholar
  53. 53.
    Stahl, Y., Wink, R.H., Ingram, G.C., and Simon, R., A signaling module controlling the stem cell niche in Arabidopsis root meristems, Curr. Biol., 2009, vol. 19, pp. 909–914.PubMedCrossRefGoogle Scholar
  54. 54.
    Gonzali, S., Novi, G., Loreti, E., Paolicchi, F., Poggi, A., Alpi, A., and Perata, P., A turanose-insensitive mutant suggests a role for WOX5 in auxin homeostasis in Arabidopsis thaliana, Plant J., 2005, vol. 44, pp. 633–645.PubMedCrossRefGoogle Scholar
  55. 55.
    Sugimoto, K., Jiao, Y., and Meyerowitz, E.M., Arabidopsis regeneration from multiple tissues occurs via a root development pathway, Dev. Cell, 2010, vol. 18, pp. 463–471.PubMedCrossRefGoogle Scholar
  56. 56.
    Che, P., Lall, S., and Howell, S.H., Developmental steps in acquiring competence for shoot development in Arabidopsis tissue culture, Planta, 2007, vol. 226, pp. 1183–1194.PubMedCrossRefGoogle Scholar
  57. 57.
    Mathesius, U., Weinman, J.J., Rolfe, B.J., and Djordjevic, M.A., Rhizobia can induce nodules in white clover by “hijacking” mature cortical cells activated during lateral root development, Mol. Plant-Microbe Interact., 2000, vol. 13, pp. 170–182.PubMedCrossRefGoogle Scholar
  58. 58.
    Searle, I.R., Men, A.E., Laniya, T.S., Buzas, D.M., Iturbe-Ormaetxe, I., Carroll, B.J., and Gresshoff, P.M., Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase, Science, 2003, vol. 299, pp. 109–112.PubMedCrossRefGoogle Scholar
  59. 59.
    Osipova, M.A., Mortier, V., Demchenko, K.N., Tsyganov, V.E., Tikhonovich, I.A., Lutova, L.A., Dolgikh, E.A., and Goormachtig, S., WUSCHEL-RELATED HOMEOBOX5 gene expression and interaction of CLE peptides with components of the systemic control add two pieces to the puzzle of autoregulation of nodulation, Plant Physiol., 2012, vol. 158, pp. 1329–1341.PubMedCentralPubMedCrossRefGoogle Scholar
  60. 60.
    Hirsch, A.M., Bhuvaneswari, T.V., Torrey, J.G., and Bisseling, T., Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors, Proc. Natl. Acad. Sci. USA, 1989, vol. 86, pp. 1244–1248.PubMedCentralPubMedCrossRefGoogle Scholar
  61. 61.
    Pawlowski, K. and Demchenko, K.N., The diversity of actinorhizal symbiosis, Protoplasma, 2012, vol. 249, pp. 967–979.PubMedCrossRefGoogle Scholar
  62. 62.
    De Buck, S., de Wilde, C., van Montagu, M., and Depicker, A., Determination of the T-DNA transfer and the T-DNA integration frequencies upon cocultivation of Arabidopsis thaliana root explants, Mol. Plant-Microbe Interact., 2000, vol. 13, pp. 658–665.PubMedCrossRefGoogle Scholar
  63. 63.
    De Almeida, E.J. and Gheysen, G., Nematodeinduced endoreduplication in plant host cells: why and how? Mol. Plant-Microbe Interact., 2013, vol. 26, pp. 17–24.CrossRefGoogle Scholar
  64. 64.
    Olsen, A.N. and Skriver, K., Ligand mimicry? Plantparasitic nematode polypeptide with similarity to CLAVATA3, Trends Plant Sci., 2003, vol. 8, pp. 55–57.PubMedCrossRefGoogle Scholar
  65. 65.
    Replogle, A., Wang, J., Bleckmann, A., Hussey, R.S., Baum, T.J., Sawa, S., Davis, E.L., Wang, X., Simon, R., and Mitchum, M.G., Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE, Plant J., 2011, vol. 65, pp. 430–440.PubMedCrossRefGoogle Scholar
  66. 66.
    Huang, G.Z., Dong, R.H., Allen, R., Davis, E.L., Baum, T.J., and Hussey, R.S., A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor, Mol. Plant-Microbe Interact., 2006, vol. 19, pp. 463–470.PubMedCrossRefGoogle Scholar
  67. 67.
    Etchells, J.P. and Turner, S.R., The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division, Development, 2010, vol. 137, pp. 767–774.PubMedCrossRefGoogle Scholar
  68. 68.
    Pernisová, M., Klíma, P., Horák, J., Válková, M., Malbeck, J., Soucek, P., Reichman, P., Hoyerová, K., Dubová, J., Friml, J., Zazímalová, E., and Hejátko, J., Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 3609–3614.PubMedCentralPubMedCrossRefGoogle Scholar
  69. 69.
    Matsumoto-Kitano, M., Kusumoto, T., Tarkowski, P., Kinoshita-Tsujimura, K., Václavíková, K., Miyawaki, K., and Kakimoto, T., Cytokinins are central regulators of cambial activity, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 20 027–20 031.CrossRefGoogle Scholar
  70. 70.
    Nieminen, K., Immanen, J., Laxell, M., Kauppinen, L., Tarkowski, P., Dolezal, K., Tähtiharju, S., Elo, A., Decourteix, M., Ljung, K., Bhalerao, R., Keinonen, K., Albert, V.A., and Helariutta, Y., Cytokinin signaling regulates cambial development in poplar, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 20 032–20 037.CrossRefGoogle Scholar
  71. 71.
    Suer, S., Agusti, J., Sanchez, P., Schwarz, M., and Greb, T., WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis, Plant Cell, 2011, vol. 23, pp. 3247–3259.PubMedCentralPubMedCrossRefGoogle Scholar
  72. 72.
    Aloni, R., Foliar and axial aspects of vascular differentiation: hypotheses and evidence, J. Plant Growth Regul., 2001, vol. 20, pp. 22–34.CrossRefGoogle Scholar
  73. 73.
    Milhinhos, A. and Miguel, C.M., Hormone interactions in xylem development: a matter of signals, Plant Cell Rep., 2013, vol. 32, pp. 867–883.PubMedCrossRefGoogle Scholar
  74. 74.
    Sachs, T., The control of patterned differentiation of vascular tissues, Adv. Bot. Res., 1981, vol. 9, pp. 151–262.CrossRefGoogle Scholar
  75. 75.
    Sauer, M., Balla, J., Luschnig, C., Wisniewska, J., Reinöhl, V., Friml, J., and Benková, E., Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity, Genes Dev., 2006, vol. 20, pp. 2902–2911.PubMedCentralPubMedCrossRefGoogle Scholar
  76. 76.
    Wenzel, C.L., Schuetz, M., Yu, Q., and Mattsson, J., Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana, Plant J., 2007, vol. 49, pp. 387–398.PubMedCrossRefGoogle Scholar
  77. 77.
    Etchells, J.P., Provost, C.M., Mishra, L., and Turner, S.R., WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organization, Development, 2013, vol. 140, pp. 2224–2234.PubMedCentralPubMedCrossRefGoogle Scholar
  78. 78.
    Fisher, K. and Turner, S., PXY, a receptor-like kinase essential for maintaining polarity during plant vasculartissue development, Curr. Biol., 2007, vol. 17, pp. 1061–1066.PubMedCrossRefGoogle Scholar
  79. 79.
    Fiers, M., Hause, G., Boutilier, K., Casamitjana-Martinez, E., Weijers, D., Offringa, R., van der Geest, L., van Lookeren, Campagne, M., and Liu, C.M., Misexpression of the CLV3/ESR-like gene CLE19 in Arabidopsis leads to a consumption of root meristem, Gene, 2004, vol. 327, pp. 37–49.PubMedCrossRefGoogle Scholar
  80. 80.
    Etchells, J.P., Provost, C.M., and Turner, S.R., Plant vascular cell division is maintained by an interaction between PXY and ethylene signaling, PLoS Genet., 2012, vol. 8: e1002997.Google Scholar
  81. 81.
    Schrader, J., Nilsson, J., Mellerowicz, E., Berglund, A., Nilsson, P., Hertzberg, M., and Sandberg, G., A highresolution transcript profile across the wood-forming meristem of poplar identifies potential regulators of cambial stem cell identity, Plant Cell, 2004, vol. 16, pp. 2278–2292.PubMedCentralPubMedCrossRefGoogle Scholar
  82. 82.
    Agusti, J., Lichtenberger, R., Schwarz, M., Nehlin, L., and Greb, T., Characterization of transcriptome remodeling during cambium formation identifies MOL1 and RUL1 as opposing regulators of secondary growth, PLoS Genet., 2011, vol. 7: e1001312.PubMedCentralPubMedCrossRefGoogle Scholar
  83. 83.
    Ohmori, Y., Tanaka, W., Kojima, M., Sakakibara, H., and Hiranoa, H.-J., WUSCHEL-RELATED HOMEOBOX4 is involved in meristem maintenance and is negatively regulated by the CLE gene FCP1 in rice, Plant Cell, 2013, vol. 25, pp. 229–241.PubMedCentralPubMedCrossRefGoogle Scholar
  84. 84.
    Truernit, E. and Haseloff, J., A role for KNAT class II genes in root development, Plant Signal. Behav., 2007, vol. 2, pp. 10–12.PubMedCentralPubMedCrossRefGoogle Scholar
  85. 85.
    Azarakhsh, M., Osipova, M., and Lutova, L., Studying the role of KNOX genes in symbiotic nodule development, Abst., 18th Int. Congr. “Nitrogen Fixation” (October 14–18, 2013, Miyazaki, Japan), Miyazaki, 2014, p. 79.Google Scholar
  86. 86.
    Mele, G., Ori, N., Sato, Y., and Hake, S., The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways, Genes Dev., 2003, vol. 17, pp. 2088–2093.PubMedCentralPubMedCrossRefGoogle Scholar
  87. 87.
    Li, E., Bhargava, A., Qiang, W., Friedmann, M.C., Forneris, N., Savidge, R.A., Johnson, L.A., Mansfield, S.D., Ellis, B.E., and Douglas, C.J., The class II KNOX gene KNAT7 negatively regulates secondary wall formation in Arabidopsis and is functionally conserved in Populus, New Phytol., 2012, vol. 194, pp. 102–115.PubMedCrossRefGoogle Scholar
  88. 88.
    Du, J., Mansfield, S.D., and Groover, A.T., The Populus homeobox gene ARBORKNOX2 regulates cell differentiation during secondary growth, Plant J., 2009, vol. 60, pp. 1000–1014.PubMedCrossRefGoogle Scholar
  89. 89.
    Rosin, F.M., Hart, J.K., Horner, H.T., Davies, P.J., and Hannapel, D.J., Overexpression of a knotted-like homeobox gene of potato alters vegetative development by decreasing gibberellin accumulation, Plant Physiol., 2003, vol. 132, pp. 106–117.PubMedCentralPubMedCrossRefGoogle Scholar
  90. 90.
    Tanaka, M., Kato, N., Nakayama, H., Nakatani, M., and Takahata, Y., Expression of class I knotted1-like homeobox genes in the storage roots of sweet potato (Ipomoea batatas), Plant Physiol., 2008, vol. 165, pp. 1726–1735.Google Scholar
  91. 91.
    Lutova, L.A., Dolgikh, E.A., Dodueva, I.E., Osipova, M.A., and Il’ina, E.L., Investigation of systemic control of plant cell division and differentiation in the model of tumor growth in radish, Russ. J. Genetics, 2008, vol. 44, pp. 936–943.CrossRefGoogle Scholar
  92. 92.
    Baima, S., Nobili, F., Sessa, G., Lucchetti, S., Ruberti, I., and Morelli, G., The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana, Development, 1995, vol. 121, pp. 4171–4182.PubMedGoogle Scholar
  93. 93.
    Donner, T.J., Sherr, I., and Scarpella, E., Auxin signal transduction in Arabidopsis vein formation, Plant Signal. Behav., 2010, vol. 5, pp. 70–72.PubMedCentralPubMedCrossRefGoogle Scholar
  94. 94.
    Ilegems, M., Douet, V., Meylan-Bettex, M., Uyttewaal, M., Brand, L., Bowman, J.L., and Stieger, P.A., Interplay of auxin, KANADI and class III HD-ZIP transcription factors in vascular tissue formation, Development, 2010, vol. 137, pp. 975–984.PubMedCrossRefGoogle Scholar
  95. 95.
    Izhaki, A. and Bowman, J.L., KANADI and class III HD-ZIP gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis, Plant Cell, 2007, vol. 19, pp. 495–508.PubMedCentralPubMedCrossRefGoogle Scholar
  96. 96.
    Kubo, M., Udagawa, M., Nishikubo, N., Horiguchi, G., Yamaguchi, M., Ito, J., Mimura, T., Fukuda, H., and Demura, T., Transcription switches for protoxylem and metaxylem vessel formation, Genes Dev., 2005, vol. 19, pp. 1855–1860.PubMedCentralPubMedCrossRefGoogle Scholar
  97. 97.
    Ohashi-Ito, K., Oda, Y., and Fukuda, H., Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation, Plant Cell, 2010, vol. 22, pp. 3461–3473.PubMedCentralPubMedCrossRefGoogle Scholar
  98. 98.
    Bonke, M., Thitamadee, S., Mähönen, A.P., Hauser, M.T., and Helariutta, Y., APL regulates vascular tissue identity in Arabidopsis, Nature, 2003, vol. 426, pp. 181–186.PubMedCrossRefGoogle Scholar
  99. 99.
    Yordanov, Y.S., Regan, S., and Busov, V., Members of the lateral organ boundaries domain transcription factor family are involved in the regulation of secondary growth in Populus, Plant Cell, 2010, vol. 22, pp. 3662–3677.PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  • I. E. Dodueva
    • 1
  • M. S. Gancheva
    • 1
  • M. A. Osipova
    • 1
  • V. E. Tvorogova
    • 1
  • L. A. Lutova
    • 1
  1. 1.Department of Genetics and Biotechnology, Faculty of BiologySt. Petersburg State UniversitySt. PetersburgRussia

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