Plant Molecular Biology

, Volume 56, Issue 6, pp 849–861 | Cite as

Molecular characterization of a WEE1 gene homologue in tomato (Lycopersicon esculentum Mill.)

  • Nathalie Gonzalez
  • Michel Hernould
  • Frédéric Delmas
  • Frédéric Gévaudant
  • Philippe Duffe
  • Mathilde Causse
  • Armand Mouras
  • Christian Chevalier


Early fruit development in tomato (Lycopersicon esculentum Mill.) proceeds in two distinct phases of growth that comprise cell division and cell expansion, respectively. In pericarp and the jelly like locular tissue of tomato fruit, the transition between cell division to cell expansion is characterized by the arrest of mitotic activity, numerous rounds of nuclear DNA endoreduplication and the inhibition of Cyclin-Dependent Kinase A (CDKA) activity. To investigate whether the WEE1 kinase may play a role during the endoreduplication process, we isolated and characterized the tomato homologue for WEE1. The LeWEE1 gene consisted of 10 exons with a predicted 510 amino acid-long protein. The accumulation of the corresponding transcripts was associated with mitotically active organs: developing fruits, seeds and roots. Interestingly, LeWEE1was expressed in the jelly like locular tissue concomitant with endoreduplication during fruit development. Using tobacco BY-2 synchronized cells, we showed that the WEE1 gene expression is cell-cycle regulated with a maximum transcript accumulation at S phase. Our data indicate the putative dual contribution of LeWEE1 in the classical cell cycle and the endocycle.


cell division cell expansion early fruit development endoreduplication tomato WEE1 



cyclin dependent kinase


days post anthesis


mature green


red ripe


reverse transcription


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  1. Bereterbide, A., Hernould, M., Farbos, I., Glimelius, K., Mouras, A. 2002Restoration of stamen development and production of functional pollen in an alloplasmic CMS tobacco line by ectopic expression of the Arabidopsis thaliana SUPERMANPlant J.29607615Google Scholar
  2. Brukhin, V., Hernould, M., Gonzalez, N., Chevalier, C., Mouras, A. 2003Flower development schedule in tomato Lycopersicon esculentum cv. sweet cherrySex Plant Reprod.15311320Google Scholar
  3. Chevalier, C., Bourgeois, E., Just, D., Raymond, P. 1996Metabolic regulation of asparagine synthetase gene expression in maize (Zea mays L.) root tipsPlant J.9111Google Scholar
  4. Criqui, M.-C., Genschik, P. 2002Mitosis in plants: how far we have come at the molecular level?Curr. Opin. Plant Biol.5487493Google Scholar
  5. De Jager, S.M., Murray, J.A.H. 1999Retinoblastoma proteins in plantsPlant Mol. Biol.41295299Google Scholar
  6. Delmas, F., Petit, J., Joubès, J., Séveno, M., Paccalet, T., Hernould, M., Lerouge, P., Mouras, A., Chevalier, C. 2003The gene expression and enzyme activity of plant 3-deoxy-D-manno-2-octulosonic acid-8-phosphate (Kdo-8-P) Synthase are preferentially associated with dividing cells in a cell-cycle dependent mannerPlant Physiol.133348360Google Scholar
  7. De Veylder, L., Joubès, J., Inzé, D. 2003Plant cell cycle transitionsCurr. Opin. Plant Biol.6536543Google Scholar
  8. Dewitte, W., Murray, J.A.H. 2003The plant cell cycleAnnu. Rev. Plant Mol. Biol.54235264Google Scholar
  9. Edgar, B.A., Orr-Weaver, T.L. 2001Endoreplication cell cycles: more for lessCell105297306CrossRefPubMedGoogle Scholar
  10. Fantes, P., Nurse, P. 1981Division timing: controls, models and mechanismsJohn, P.C.L. eds. The Cell CycleCambridge University PressCambridge1133Google Scholar
  11. Florea, L., Hartzell, G., Zhang, Z., Rubin, G.M., Miller, W. 1998A computer program for aligning a cDNA sequence with a genomic DNA sequenceGenome Res.8967974Google Scholar
  12. Gattiker, A., Gasteiger, E., Bairoch, A. 2002Scan Prosite: a reference implementation of a PROSITE scannig toolAppl. Bioinformat.1107108Google Scholar
  13. Germain, V., Raymond, P., Ricard, B. 1997Differential expression of two tomato lactate deshydrogenase genes in response to oxygen deficitPlant Mol. Biol.35711721Google Scholar
  14. Gillaspy, G., Ben-David, H., Gruissem, W. 1993Fruits: a developmental perspectivePlant Cell514391451CrossRefPubMedGoogle Scholar
  15. Gutierrez, C., Ramirez-Parra, E., Mar-Castellano, M., Carlos del Pozo, J. 2002G1 to S transition : more than a cell cycle engine switchCurr. Opin. Plant Biol.5480486Google Scholar
  16. Harvey, S.L., Kellog, D.R. 2003Conservation of mechanisms controlling entry into mitosis: budding yeast Wee1 delays entry into mitosis and is required for cell size controlCurr. Biol.13264275Google Scholar
  17. Joubès, J., Chevalier, C. 2000Endoreduplication in higher plantsPlant. Mol. Biol.43737747Google Scholar
  18. Joubès, J., Chevalier, C., Dudits, D., Heberle-Bors, E., Inzé, D., Umeda, M., Renaudin, J.-P. 2000Cyclin-dependent kinases related protein kinases in plantsPlant. Mol. Biol.43607621Google Scholar
  19. Joubès, J., Lemaire-Chamley, M., Delmas, F., Walter, J., Hernould, M., Mouras, A., Raymond, P., Chevalier, C. 2001A new C-type Cyclin-Dependent Kinase from tomato expressed in dividing tissues does not interact with mitotic and G1 cyclinsPlant Physiol.12614031415Google Scholar
  20. Joubès, J., Phan, T.-H., Just, D., Rothan, C., Bergounioux, C., Raymond, P., Chevalier, C. 1999Molecular and biochemical characterization of the involvement of Cyclin-Dependent Kinase CDKA during the early development of tomato fruitPlant Physiol.121857869Google Scholar
  21. Joubès, J., Walsh, D., Raymond, P., Chevalier, C. 2000bMolecular characterization of the expression of distinct classes of cyclins during the early development of tomato fruitPlanta211430439Google Scholar
  22. Larkins, B.A., Dilkes, B.P., Dante, R.A., Coelho, C.M., Woo, Y.-M., Liu, Y. 2001Investigating the hows and whys of DNA endoreduplicationJ. Exp. Bot.52183192Google Scholar
  23. Landrieu, I., da Costa, M., De Veylder, L., Dewitte, F., Vandepoele, K., Hassan, S., Wieruszeski, J.-M., Faure, J.-D., Van Montagu, M., Inzé, D. and Lippens, G. 2004. A small CDC25 dual-specificity tyrosine-phosphatase isoform in Arabidopsis thaliana. 101: 13380–13385Google Scholar
  24. Lew, D.J. 2000Cell cycle checkpoints that ensure coordination between nuclear and cytoplasmic events in Saccharomyces cerevisiaeCurr. Opin. Genet. Dev.104753Google Scholar
  25. Liu, X.C., Dickinson, H.G. 1989Cellular energy levels and their effect on cytoplasmic male cell abortion in cytoplasmic male sterile lines of petunia hybridaSex Plant Reprod.2167172Google Scholar
  26. Mironov, V., De Veylder, L., Van Montagu, M., Inzé, D. 1999Cyclin-dependent kinases and cell division in plants- the nexusPlant Cell11509522Google Scholar
  27. Menges, M, Hennig, L., Gruissem, W., Murray, J.A. 2003Genome-wide gene expression in an Arabidopsis cell suspensionPlant Mol. Biol.53423442Google Scholar
  28. Nakai, K., Kanehisa, M. 1991Expert system for predicting protein localization sites in gram-negative bacteriaProteins1195110PubMedGoogle Scholar
  29. Pan, Q., Liu, Y.-S., Budai-Hadrian, O., Sela, M., Carmel-Goren, L., Zamir, D., Fluhr, R. 2000Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and ArabidopsisGenetics155309322PubMedGoogle Scholar
  30. Porceddu, A., Stals, H., Reichheld, J.-P., Segers, G., De Veylder, L., Pinho Barroco, R., Casteels, P., Van Montagu, M., Inzé, D., Mironov, V. 2001A plant-specific cyclin-dependent kinase is involved in the control of G2/M progression in plantsJ. Biol. Chem.2763635436360Google Scholar
  31. Renaudin, J.-P., Doonan, J.H., Freeman, D., Hashimoto, J., Hirt, H., Inzé, D., Jacobs, T., Kouchi, H., Rouzé, P., Sauter, M., Savouré, A., Sorrell, D.A., Sundaresan, V., Murray, J.A. 1996Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organizationPlant Mol. Biol.3210031018Google Scholar
  32. Russell, P., Nurse, P. 1987Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homologCell49559567Google Scholar
  33. Sambrook, J., Fritsch, E.F., Maniatis, F. 1989Molecular Cloning: a Laboratory Manual, 2nd ednCold Spring Harbor LaboratoryNew-YorkGoogle Scholar
  34. Sorrell, D.A., Marchbank, A., McMahon, K., Dickinson, J.R., Rogers, H.J., Francis, D. 2002A WEE1 homologue from Arabidopsis thalianaPlanta215518522Google Scholar
  35. Sugimoto-Shirasu, K., Roberts, K. 2003“Big it up”: endoreduplication and cell-size control in plantsCurr. Opin. Plant Biol.6544553Google Scholar
  36. Sun, Y., Dilkes, B.P., Zhang, C., Dante, R.A., Carneiro, N.P., Lowe, K.S., Jung, R., Gordon-Kamm, W.J., Larkins, B.A. 1999Characterization of maize (Zea mays L.) Wee1 and its activity in developig endospermProc. Natl. Acad. Sci. USA9641804185Google Scholar
  37. Vallejos, C.E., Sakiama, N.S., Chase, C.D. 1992A molecular marker-based linkage map of Phaseolus vulgaris LGenetics131733740Google Scholar
  38. Vandepoele, K., Raes, J., De Veylder, L., Rouzé, P., Rombauts, S., Inzé, D. 2002Genome-wide analysis of core cell-cycle genes in ArabidopsisPlant Cell14903916CrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Nathalie Gonzalez
    • 1
  • Michel Hernould
    • 1
  • Frédéric Delmas
    • 1
  • Frédéric Gévaudant
    • 1
  • Philippe Duffe
    • 2
  • Mathilde Causse
    • 2
  • Armand Mouras
    • 1
  • Christian Chevalier
    • 1
  1. 1.Unité Mixte de Recherche en Physiologie et Biotechnologie Végétales Institut de Biologie Végétale Intégrative, Institut National de la Recherche AgronomiqueInstitut National de la Recherche Agronomique et Universités de Bordeaux 1 et Victor Segalen-Bordeaux 2CedexFrance
  2. 2.Unité de Génétique et Amélioration des Fruits et LégumesInstitut National de la Recherche AgronomiquecedexFrance

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