Plant Biol (Stuttg) 2006; 8(3): 389-396
DOI: 10.1055/s-2006-923797
Review Article

Georg Thieme Verlag Stuttgart KG · New York

Crosstalk between Auxin, Cytokinins, and Sugars in the Plant Cell Cycle

K. Hartig1 , E. Beck1
  • 1Department of Plant Physiology, University of Bayreuth, Universitätsstraße 30, 95440 Bayreuth, Germany
Further Information

Publication History

Received: September 13, 2005

Accepted: November 18, 2005

Publication Date:
13 March 2006 (online)

Abstract

Plant meristems are utilization sinks, in which cell division activity governs sink strength. However, the molecular mechanisms by which cell division activity and sink strength are adjusted to a plant's developmental program in its environmental setting are not well understood. Mitogenic hormonal as well as metabolic signals drive and modulate the cell cycle, but a coherent idea of how this is accomplished, is still missing. Auxin and cytokinins are known as endogenous mitogens whose concentrations and timing, however, can be externally affected. Although the sites and mechanisms of signal interaction in cell cycle control have not yet been unravelled, crosstalk of sugar and phytohormone signals could be localized to several biochemical levels. At the expression level of cell cycle control genes, like cyclins, Cdks, and others, synergistic but also antagonistic interactions could be demonstrated. Another level of crosstalk is that of signal generation or modulation. Cytokinins affect the activity of extracellular invertases and hexose-uptake carriers and thus impinge on an intracellular sugar signal. With tobacco BY-2 cells, a coordinated control of cell cycle activity at both regulatory levels could be shown. Comparison of the results obtained with the root cell-representing BY-2 cells with literature data from shoot tissues or green cell cultures of Arabidopsis and Chenopodium suggests opposed and tissue-specific regulatory patterns of mitogenic signals and signal crosstalk in root and shoot meristems.

References

  • 1 Balibrea Lara M. E., Gonzalez Garcia M.-C., Fatima T., Ehness R., Lee T.K., Tanner W., Roitsch T.. Extracellular invertase is an essential component of cytokinin-mediated delay of senescence.  Plant Cell. (2004);  16 1276-1287
  • 2 Beck E.. Towards an understanding of plant growth regulation: cytokinins as major signals for biomass distribution. Strnad, M., Pec, P., and Beck, E., eds. Advances in Regulation of Plant Growth and Development. Prague; Peres Publishers (1999): 97-110
  • 3 Beck E., Wagner B.M.. Quantification of the daily cytokinin transport from the root to the shoot of Urtica dioica L.  Botanica Acta. (1994);  107 342-348
  • 4 Berleth T., Krogan N. T., Scapella E.. Auxin signals - turning genes on and turning cells around.  Current Opinion in Plant Biology. (2004);  7 553-563
  • 5 Blilou I., Frugier F., Folmer S., Serralbo O., Willemsen V., Wolkenfelt H., Eloy N. B., Ferreira P. C., Weisbeck P., Scheres B.. The Arabidopsis HOBBIT gene encodes a CDC27 homolog that links the plant cell cycle to progression of cell differentiation.  Genes and Development. (2002);  16 566-575
  • 6 Callard D., Axelos M., Mazzolini L.. Novel molecular markers for late phase of the growth cycle of Arabidopsis thaliana cell-suspension cultures are expressed during organ senescence.  Plant Physiology. (1996);  112 705-715
  • 7 Cockcroft C. E., Den Boer B. G. W., Healy J. M. S., Murray J. A. H.. Cyclin D control of growth rate in plants.  Nature. (2000);  405 575-579
  • 8 Coenen C., Lomax T. L.. Auxin-cytokinin interactions in higher plants: old problems and new tools.  Trends in Plant Science. (1997);  2 351-356
  • 9 Dharmasiri N., Dharmasiri S., Estelle M.. The F‐box protein TIR1 is an auxin receptor.  Nature. (2005);  435 441-445
  • 10 Del Pozo J. C., Boniotti M. B., Guitierrez C.. Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF (AtSKP2) pathway in response to light.  Plant Cell. (2002);  14 3057-3071
  • 11 Del Pozo J. C., Lopez-Matas M. A., Ramirez-Parra E., Guitierrez C.. Hormonal control of the plant cell cycle.  Physiologia Plantarum. (2005);  123 173-183
  • 12 Dewitte W., Chiappetta A., Azmi A., Witters E., Strnad M., Rembur J., Noin M., Chriqiu D., Van Onckelen H.. Dynamics of cytokinins in apical shoot meristems of a day-neutral tobacco during floral transition and flower formation.  Plant Physiology. (1999);  119 111-121
  • 13 Dobrev P., Motyka V., Gaudinova A., Malbeck J., Travnickova A., Kaminek M., Vankova R.. Transient accumulation of cis- and trans-zeatin type cytokinins and its relation to cytokinin oxidase activity during cell cycle of synchronized tobacco BY‐2 cells.  Plant Physiology and Biochemistry. (2003);  40 333-337
  • 14 Ehness R., Roitsch T.. Co-ordinated induction of mRNAs for extracellular invertase and a glucose transporter in Chenopodium rubrum by cytokinins.  The Plant Journal. (1997);  11 539-548
  • 15 Friml J., Benkova E., Blilou I., Wisniewska J., Hamann T., Ljung K., Woody S., Sandberg G., Scheres B., Jurgens G., Palme K.. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis.  Cell. (2002);  108 661-673
  • 16 Goetz M., Goedt D. E., Roitsch T.. Tissue-specific induction of the mRNA for an extracellular invertase isoenzyme of tobacco by brassinosteroids suggests a role for steroid hormones in assimilate partitioning.  The Plant Journal. (2000);  22 515-522
  • 17 Hartig K., Beck E.. Endogenous cytokinin oscillations control cell cycle progression of tobacco BY‐2 cells.  Plant Biology. (2005 a);  7 33-41
  • 18 Hartig K., Beck E.. Assessment of lovastatin application as tool in probing cytokinin-mediated cell cycle regulation.  Physiologia Plantarum. (2005 b);  125 260-267
  • 19 Hartig K.. Zellteilungsregulation meristematischer Wurzelzellen (Tabak BY‐2) durch Phytohormone und Zucker. PhD Thesis, University of Bayreuth. (2005)
  • 20 Heyer A. G., Raap M., Schroeer B., Marty B., Willmitzer L.. Cell wall invertase expression at the apical meristem alters floral, architectural, and reproductive traits in Arabidopsis thaliana.  The Plant Journal. (2004);  39 161-169
  • 21 Himanen K., Boucheron E., Vanneste S., De Almeida Engler J., Inzé D., Beeckman T.. Auxin-mediated cell cycle activation during early lateral root initiation.  Plant Cell. (2002);  14 2339-2351
  • 22 Ho L. C.. Metabolism and compartmentation of imported sugars in sink organs in relation to sink strength.  Annual Review of Plant Physiology and Plant Molecular Biology. (1988);  39 355-378
  • 23 Houssa C., Bernier G., Pieltain A., Kinet J. M., Jaqumard A.. Activation of latent DNA-replication origins - a universal effect of cytokinins.  Planta. (1994);  193 247-250
  • 24 Howell S. H., Lall S., Che P.. Cytokinins and shoot developments.  Trends in Plant Science. (2003);  8 453-459
  • 25 Hwang I., Sheen J.. Two-component circuitry in Arabidopsis cytokinin signal transduction.  Nature. (2001);  413 383-389
  • 26 Inzé D.. Green light for the cell cycle.  EMBO Journal. (2005);  24 657-662
  • 28 John P. C. L., Zhang K., Dong C., Diederich L., Wightman F.. P34-cdc2 related proteins in control of cell cycle progression, the switch between division and differentiation in tissue development, and stimulation of division by auxin and cytokinin.  Australian Journal of Plant Physiology. (1993);  20 503-526
  • 29 Joubés J., Chevalier C.. Endoreduplication in higher plants.  Plant Molecular Biology. (2000);  43 735-745
  • 30 Kakimoto T.. Perception and signal transduction of cytokinins.  Annual Review of Plant Physiology and Plant Molecular Biology. (2003);  54 605-627
  • 31 Kuiper D., Schuit J., Kuiper P. J. C.. Effects of internal and external cytokinin concentrations on root growth and shoot to root ratio of Plantago major ssp. pleiosperma at different nutrient conditions.  Plant and Soil. (1988);  111 231-236
  • 32 Laureys F., Smets R., Lenjou M., Van Bockstaele D., Inzé D., Van Onckelen H.. A low content in zeatin type cytokinins is not restrictive for the occurrence of G1/S transition in tobacco BY‐2 cells.  FEBS Letters. (1999);  460 123-128
  • 33 León P., Sheen J.. Sugar and hormone connections.  Trends in Plant Science. (2003);  8 110-116
  • 34 Long J. C., Zhao W., Rashotte A. M., Muday G. K., Huber S. C.. Gravity stimulated changes in auxin and invertase gene expression in maize pulvinal cells.  Plant Physiology. (2002);  128 591-602
  • 35 Miller C. O., Skoog F., Okumura F. S., Von Saltza M., Strong F. W.. Isolation, structure and synthesis of kinetin, a substance promoting cell division.  Journal of the American Chemical Society. (1956);  11 118-131
  • 36 Mironov V., De Veylder L., Van Montagu M., Inzé D.. Cyclin-dependent kinases and cell division in plants - the nexus.  Plant Cell. (1999);  11 509-521
  • 37 Miyawaki K., Matsumoto-Kitano M., Kakimoto T.. Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin and nitrate.  The Plant Journal. (2004);  37 128-138
  • 38 Planchais S., Glab N., Tréhin C., Perennes C., Bureau J.-M., Meijer L., Bergounioux C.. Roscovitine, a novel cyclin-dependent kinase inhibitor, characterizes restriction point and G2/M transition in tobacco BY‐2 cell suspension.  The Plant Journal. (1997);  12 191-202
  • 39 Rashotte A. M., Sook Chae H., Maxwell B. B., Kieber J. J.. The interaction of cytokinin with other signals.  Physiologia Plantarum. (2005);  123 184-194
  • 40 Redig P., Shaul O., Inzé D., Van Montagu M., Van Onckelen H.. Levels of endogenous cytokinins, indole-3-acetic acid and abscisic acid during the cell cycle of synchronized tobacco BY‐2 cells.  FEBS Letters. (1996);  391 175-180
  • 41 Reichheld J.-P., Chaubet N., Shen W. H., Renaudin J.-P., Gigot C.. Multiple A-type cyclins express sequentially during the cell cycle in Nicotiana tabacum BY2 cells.  Proceedings of the National Academy of Sciences of the USA. (1996);  93 13819-13824
  • 42 Renaudin J.-P., Doonan J. H., Freeman D., Hashimoto J., Hirt H., Inzé D., Jacobs T., Kouchi H., Rouze P., Sauter M., Savoure A., Sorrell D. A., Sundaresan V., Murray J. A. H.. Plant cyclins: a unified nomenclature for plant A-, B- and D-cyclins based on sequence organisation.  Plant Molecular Biology. (1996);  32 1003-1018
  • 43 Richard C., Lescot M., Inzé D., De Veylder L.. Effect of auxin, cytokinin, and sucrose on cell cycle gene expression in Arabidopsis thaliana cell suspension cultures.  Plant Cell, Tissue and Organ Culture. (2002);  69 167-176
  • 44 Riou-Khamlichi C., Huntley R., Jacqumard A., Murray J. A. H.. Cytokinin activation of Arabidopsis cell division through a D-type cyclin.  Science. (1999);  283 1541-1544
  • 45 Roitsch T., Ehness R.. Regulation of source/sink relations by cytokinins.  Plant Growth Regulation. (2000);  32 359-367
  • 46 Shen W.-H.. The plant E2F‐Rb pathway and epigenic control.  Trends in Plant Science. (2002);  7 505-511
  • 47 Sheen J., Zhou L., Jang J. C.. Sugars as signalling molecules.  Current Opinion in Plant Biology. (1999);  2 410-508
  • 48 Sherson S. M., Alford H. L., Forbes S. M., Wallac G., Smith S. M.. Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis.  Journal of Experimental Botany. (2003);  54 525-531
  • 49 Smalle J., Kurepa J., Yang P., Babiychuk E., Kushnir S., Durski A., Vierstra R. D.. Cytokinin growth responses in Arabidopsis involve the 26S proteasom subunit RPN12.  Plant Cell. (2002);  14 17-32
  • 50 Soni R., Carmichael J. P., Shah Z. H., Murray J. A. H.. A family of cyclin D homologues from plant differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif.  Plant Cell. (1995);  7 85-103
  • 51 Sorrell D. A., Combettes B., Chaubet-Gigot N., Gigot C., Murray J. A. H.. Distinct cyclin D genes show mitotic accumulation or constant levels of transcripts in tobacco BY‐2 cells.  Plant Physiology. (1999);  119 343-351
  • 52 Sorrell D. A., Menges M., Healy J. M., Deveaux Y., Amano C., Su Y., Nakagami H., Shinmyo A., Doonan J. H., Sekine M., Murray J. A. H.. Cell cycle regulation of cyclin-dependent kinases in tobacco cultivar Bright Yellow-2 cells.  Plant Physiology. (2001);  126 1214-1223
  • 53 Valdes O.. Die Bedeutung von endogenem und künstlichem Auxin für die Kultivierung photoautotropher Zellen von Chenopodium rubrum. PhD Thesis, University of Bayreuth. (2005)
  • 54 Vanneste S., Maes L., De Smet I., Himanen K., Naudts M., Inzé D., Beeckman T.. Auxin regulation of the cell cycle and its role during lateral root initiation.  Physiologia Plantarum. (2005);  123 139-146
  • 55 Werner T., Motyka V., Laucou V., Smets R., Van Onckelen H., Schmülling T.. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity.  Plant Cell. (2003);  15 2532-2550
  • 56 Winicur Z. M., Zhang G. F., Staehelin L. A.. Auxin deprivation induces synchronous Golgi differentiation in suspension-cultured tobacco BY‐2 cells.  Plant Physiology. (1998);  117 501-513
  • 57 Wobus U., Weber H.. Sugars as signal molecules in plant seed development.  Journal of Biological Chemistry. (1999);  380 937-944
  • 58 Yonekura-Sakakibara K., Koijma M., Yamaya T., Sakibara H.. Molecular characterization of cytokinin-responsive histidin kinases in maize. Differential ligand preferences and response to cis-Zeatin.  Plant Physiology. (2004);  134 1654-1661
  • 59 Yu Y., Steinmetz A., Meyer D., Brown S., Shen W.-H.. The tobacco A-type cyclin, Nicta;CYCA3; 2, at the nexus of cell division and differentiation.  Plant Cell. (2003);  15 2763-2777
  • 60 Zhang K., Diederich L., John P. C. L.. The cytokinin requirement for cell division in cultured Nicotiana plumbaginifolia cells can be satisfied by yeast Cdc25 protein tyrosine phosphatase. Implications for mechanisms of cytokinin response and plant development.  Plant Physiology. (2005);  137 308-316

K. Hartig

Department of Plant Physiology
University of Bayreuth

Universitätsstraße 30

95440 Bayreuth

Germany

Email: katja.hartig@uni-bayreuth.de

Guest Editor: R. Reski