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The Arabidopsis leaf as a model system for investigating the role of cell cycle regulation in organ growth

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Abstract

The role of cell cycle regulation and cell division in plant growth and organ development is controversial. Some experimental data are most easily interpreted from the ‘cellular perspective’ that cell division drives growth, whereas other observations are more consistent with the ‘organismal perspective’ that cell division is merely a consequence of growth, and to a large extent facultative. Here we develop a model of cell cycle regulation in the context of leaf development based on literature, published kinematic analysis, flow-cytometric and transcriptomic data obtained from growing Arabidopsis leaves. We tested this model by comparing the in silico inhibition of the cell cycle progression with the experimental observations of transgenic plants overexpressing the cell cycle inhibitor Arath;KRP2. The model simulates the behaviour of proliferating cells quite well, but is inadequate in describing the effects on expanding cells. This may point to a difference in the nature of the expansion process during the proliferating and non-dividing phase of leaf development.

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References

  • Beemster GTS, Fiorani F, Inzé D (2003) Cell cycle: the key to plant growth control? Trends Plant Sci 8:154–158

    Article  PubMed  Google Scholar 

  • Beemster GTS, De Veylder L, Vercruysse S, West G, Rombaut D, Van Hummelen P, Galichet A, Gruissem W, Inze D, Vuylsteke M (2005) Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol 138:734–743

    Article  PubMed  Google Scholar 

  • Boudolf V, Vlieghe K, Beemster GTS, Magyara Z, Torres Acosta J-A, Maes S, Van der Schueren E, Inzé D, De Veylder L (2004) The plant-specific cyclin-dependent kinase CDKB1;1 and transcription factor E2Fa-DPa control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis. Plant Cell 16:2683–2692

    Article  PubMed  Google Scholar 

  • De Veylder L, Beeckman T, Beemster GTS, Krols L, Terras F, Landrieu I, Van der Schueren E, Maes S, Naudts M, Inzé D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13:1653–1668

    Article  PubMed  Google Scholar 

  • De Veylder L, Beeckman T, Beemster GTS, de Almeida Engler J, Ormenese S, Maes S, Naudts M., Van der Schueren E, Jacqmard A, Engler G, Inzé D (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J 21:1360–1368

    Article  PubMed  Google Scholar 

  • De Veylder L, Joubes J, Inze D (2003) Plant cell cycle transitions. Curr Opin Plant Biol 6:536–543

    Article  PubMed  Google Scholar 

  • Dewitte W, Murray JA (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264

    Article  PubMed  Google Scholar 

  • Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419

    Article  PubMed  Google Scholar 

  • Hall MN, Raff M, Thomas G (2004) Cell growth Control of cell size. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Inze D (2005) Green light for the cell cycle. EMBO J 24:657–662

    Article  PubMed  Google Scholar 

  • Ivanov VB (1971) Critical size of the cell and its transition to division. Soviet J Dev Biol 2:421–428

    Google Scholar 

  • Maere S, Heymans K, Kuiper M (2005) BiNGO: a cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21:3448–3449

    Article  PubMed  Google Scholar 

  • Melaragno JE, Mehrotra B, Coleman AW (1993) Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5:1661–1668

    Article  PubMed  Google Scholar 

  • Neufeld TP, Edgar BA (1998) Connections between growth and the cell cycle. Curr Opin Cell Biol 10:784–790

    Article  PubMed  Google Scholar 

  • Tsukaya H (2002) Interpretation of mutants in leaf morphology: genetic evidence for a compensatory system in leaf morphogenesis that provides a new link between cell and organismal theories. Int Rev Cytol 217:1–39

    PubMed  Google Scholar 

  • Vandepoele K, Raes J, De Veylder L, Rouzé P, Rombouts S, Inzé D (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14:903–916

    Article  PubMed  Google Scholar 

  • Vercruysse S, Kuiper MTR (2004) Simulating genetic networks made easy: network construction with simple building blocks. Bioinformatics (DOI: 10.1093/bioinformatics/bth478)

  • Vlieghe K, Boudolf V, Beemster GTS, Maes S, Magyar Z, Atanassova A, de Almeida Engler J, De Groodt R, Inz D, De Veylder L (2005) The DP-E2F-like gene DEL1 controls the endocycle in Arabidopsis thaliana. Curr Biol 15:59–63

    Article  PubMed  Google Scholar 

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Correspondence to Gerrit T. S. Beemster.

Appendix

Appendix

Definition of a SIM-plex program simulating the integration of cell cycle regulation into leaf growth in response to a declining availability of a growth factor. Overexpression of an inhibitor is simulated by increasing DNA duplication and mitosis (values indicated in parentheses).

 

comp GrowthFactor 100 0.006

comp CellArea 100 0.0 blackcomp

comp DNA 2 0.0

comp CellNo 1 0.0

comp CycD

comp CDKA 1000 0.0 noplot

comp SPF 5

comp CDKB noplot

comp CycB noplot

comp MPF 10

mathcomp Ratio = CellArea/DNA

mathcomp LeafArea = CellNo * CellArea

timepoints 1 to 1000

// Growth module, both lines work additive

if GrowthFactor > 1 then CellArea 2

if GrowthFactor > 25 then CellArea 2

// S-phase module

if Ratio > 50 then CycD 1

if true then transform (CDKA CycD) to SPF 5

trigger if SPF > 5 (15) then DNA = DNA * 2

// M-phase module

if GrowthFactor > 25 and DNA >= 4 then CDKB 2

if GrowthFactor > 1 and DNA >= 4 then CycB 2

if true then transform (CDKB CycB) to MPF 5

trigger if MPF > 10 (15) then CellArea = CellArea / 2

trigger if MPF > 10 (15) then DNA = DNA / 2

trigger if MPF > 10 (15) then CellNo = CellNo * 2

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Beemster, G.T.S., Vercruysse, S., De Veylder, L. et al. The Arabidopsis leaf as a model system for investigating the role of cell cycle regulation in organ growth. J Plant Res 119, 43–50 (2006). https://doi.org/10.1007/s10265-005-0234-2

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  • DOI: https://doi.org/10.1007/s10265-005-0234-2

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