Cytokinin Activation of Arabidopsis Cell Division Through a D-Type Cyclin
10.1126/science.283.5407.1541
Crossref journal-article
American Association for the Advancement of Science (AAAS)
Science (221)
Abstract

Cytokinins are plant hormones that regulate plant cell division. The D-type cyclin CycD3 was found to be elevated in a mutant of Arabidopsis with a high level of cytokinin and to be rapidly induced by cytokinin application in both cell cultures and whole plants. Constitutive expression of CycD3 in transgenic plants allowed induction and maintenance of cell division in the absence of exogenous cytokinin. Results suggest that cytokinin activates Arabidopsis cell division through induction of CycD3 at the G 1 -S cell cycle phase transition.

Bibliography

Riou-Khamlichi, C., Huntley, R., Jacqmard, A., & Murray, J. A. H. (1999). Cytokinin Activation of Arabidopsis Cell Division Through a D-Type Cyclin. Science, 283(5407), 1541–1544.

Authors 4
  1. Catherine Riou-Khamlichi (first)
  2. Rachael Huntley (additional)
  3. Annie Jacqmard (additional)
  4. James A.H. Murray (additional)
References 42 Referenced 638
  1. 10.1021/ja01610a105
  2. D. S. Letham P. B. Goodwin T. J. V. Higgins Eds. Phytohormones and Related Compounds: A Complete Treatise vol. II (Elsevier/North-Holland Amsterdam 1978).
  3. 10.1105/tpc.9.7.1021
  4. ; H. Kende and J. A. D. Zeevaart ibid. p. 1197; W. M. Gray and M. Estelle Curr. Opin. Biotechnol. 9 196 (1998). (10.1105/tpc.9.7.1197)
  5. 10.1007/BF00384976
  6. Zhang K., Letham D. S., John P. C. L., ibid. 200, 2 (1996). / ibid. by Zhang K. (1996)
  7. A. Jacqmard C. Houssa G. Bernier in Cytokinins. Chemistry Activity and Function D. W. S. Mok and M. C. Mok Eds. (CRC Boca Raton FL 1994) pp. 197–215.
  8. Nagata T., Ishida S., Hasezawa S., Takahashi Y., Int. J. Dev. Biol. 38, 321 (1994). / Int. J. Dev. Biol. by Nagata T. (1994)
  9. M. W. Bayliss in The Cell Division Cycle in Plants J. A. Bryant and D. Francis Eds. (Cambridge Univ. Press Cambridge 1985) pp. 157–177.
  10. 10.1016/0092-8674(93)90636-5
  11. ; Trends Biochem Sci. 20 187 (1995) (10.1016/S0968-0004(00)89005-2)
  12. Soni R., Carmichael J., Shah Z., Murray J. A. H., Plant Cell 7, 85 (1995). / Plant Cell by Soni R. (1995)
  13. M. Dahl et al. ibid. p. 1847.
  14. 10.1104/pp.103.2.621
  15. Fuerst R. A. U. A., Soni R., Murray J. A. H., Lindsey K., ibid. 112, 1023 (1996). / ibid. by Fuerst R. A. U. A. (1996)
  16. Arabidopsis thaliana Landsberg erecta suspension culture was maintained by weekly 20-fold dilution (12 13). Early stationary phases (day 7 after previous subculture) were filtered and washed five times with 200 ml of Murashige and Skoog (MS) medium (containing 3% sucrose but lacking auxin and cytokinin) and maintained in this medium for 24 hours before addition of inducing agents at time T = 0 and sampling at times indicated. Identical results were obtained with exponential (day 3) cells similarly treated. Chx (100 μM) was added 1 hour before other inducers and effectively prevents protein synthesis in Arabidopsis [
  17. 10.1006/jmbi.1995.0454
  18. 10.1007/BF00262641
  19. Transgenic Arabidopsis seedlings carrying the CycD3 promoter linked to a GUS reporter gene treated with zeatin also showed twofold to sevenfold induction of GUS but no change in its spatial distribution.
  20. Longitudinal sections (8 μm) of 8-week-old vegetative A. thaliana Columbia grown under short days hybridized as described [
  21. 10.1046/j.1365-313X.1996.10040601.x
  22. ] to 800-nucleotide antisense or full-length sense CycD3 35 S-uridine triphosphate–labeled riboprobes (Promega) were viewed in dark field (autoradiographic signal) or fluorescence (calcofluor staining). For cytokinin induction 50 μM BAP (Sigma) was applied daily to the apical bud for five successive days.
  23. 10.1016/S0092-8674(00)80239-1
  24. Calli were induced by Agrobacterium -mediated transformation of Arabidopsis roots as described (20) with a construct expressing CycD3 under the CaMV 35 S promoter. Calli expressed high levels of CycD3 by Northern (RNA) blot (22) but could not be regenerated.
  25. 10.1046/j.1365-313X.1995.08050637.x
  26. The CycD3 cDNA without 5′ untranslated region (UTR) was cloned in conditional vector pFLP-SWITCH (G. D. Davies N. J. Kilby C. Riou-Khamlichi J. A. H. Murray in preparation) and crossed to an hsp-FLP line (20). F1 embryos were heat shocked 3 days after pollination and F2 seeds from individual F1 plants were analyzed for reduced GUS transmission. F2 plants from such parents were tested for transmission of activated CycD3 expression and absence of hsp-FLP (see supplementary material available at www.sciencemag.org/feature/data/985481.shl).
  27. C. Riou-Khamlichi A. Jacqmard J. A. H. Murray data not shown.
  28. Explants cut from rosette leaves of 3-week-old F3 CycD3-expressing and wild-type plants were placed on MS medium with 0.45 μM 2 4-dichlorophenoxyacetic acid (2 4-D) or 2 4-D and 0.44 μM BAP (control). Calli were propagated and trimmed every 10 days; trimming was unnecessary for wild-type calli on medium lacking cytokinin.
  29. 10.1126/science.274.5289.982
  30. 10.1104/pp.119.1.343
  31. 10.1007/BF00192938
  32. 10.1007/BF02115959
  33. 10.1016/0014-5793(96)00728-4
  34. Laureys F., et al., ibid. 426, 29 (1998). / ibid. by Laureys F. (1998)
  35. RNA blots on GeneScreen Plus (NEN) were stained with methylene blue to confirm equal loading hybridized at 42°C and washed (CycD3 blots: 0.1% standard saline citrate and 0.1% SDS at 42°C for 20 min and at 65°C for 10 min; Arabidopsis histone H4 blots: 42°C for 10 min and 55°C for 10 min).
  36. Isoprenoid cytokinin determinations by enzyme-linked immunosorbent assay (ELISA) were carried out as described [
  37. 10.1016/0031-9422(91)83623-S
  38. ] with SepPak purified extracts of 10-day-old seedlings grown in liquid MS medium. Five ELISA determinations were carried out for at least two separate extractions.
  39. 10.1104/pp.98.2.621
  40. 10.1046/j.1365-313X.1995.7020245.x
  41. Cells were rendered quiescent by incubation of day 7 cells in sucrose-free medium (with hormones) for 24 hours followed by readdition of 3% sucrose at T = 0 and sampling at times indicated (C. Riou-Khamlichi and J. A. H. Murray in preparation). Incorporation of [ 3 H]thymidine into acid-insoluble material was measured in triplicate relative to background as described (10).
  42. We thank colleagues for helpful suggestions; N. Kilby G. Davies and A. Sessions for advice on the FLP activation system; L. Dehon for in situ hybridizations; D. Hanke for advice and assistance with cytokinin assays; I. Furner for Arabidopsis mutants; and A. Inskip for technical assistance. Support of Biotechnology and Biological Sciences Research Council grant P05114 and Pôles d'attraction interuniversitaires belges (Service du Premier Ministre Services fédéraux des Affaires scientifiques techniques et culturelles) P4/15 is acknowledged.
Dates
Type When
Created 23 years, 1 month ago (July 27, 2002, 5:40 a.m.)
Deposited 1 year, 7 months ago (Jan. 13, 2024, 12:05 a.m.)
Indexed 16 hours, 33 minutes ago (Aug. 30, 2025, 12:38 p.m.)
Issued 26 years, 5 months ago (March 5, 1999)
Published 26 years, 5 months ago (March 5, 1999)
Published Print 26 years, 5 months ago (March 5, 1999)
Funders 0

None

@article{Riou_Khamlichi_1999, title={Cytokinin Activation of Arabidopsis Cell Division Through a D-Type Cyclin}, volume={283}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.283.5407.1541}, DOI={10.1126/science.283.5407.1541}, number={5407}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Riou-Khamlichi, Catherine and Huntley, Rachael and Jacqmard, Annie and Murray, James A.H.}, year={1999}, month=mar, pages={1541–1544} }