Journal of Plant Research

, Volume 116, Issue 3, pp 233–239 | Cite as

Biosynthesis of cytokinins

JPR Symposium

Abstract

Cytokinins are adenine derivatives with an isoprenoid side chain and play an essential role in plant development. Plant isopentenyltransferases that catalyze the first and rate-limiting steps of cytokinin biosynthesis have recently been identified. Unlike bacterial enzymes, which catalyze the transfer of the isopentenyl moiety from dimethylallyldiphosphate (DMAPP) to the N6 position of adenosine 5′-monophosphate (AMP), plant enzymes catalyze the transfer of the isopentenyl moiety from DMAPP preferentially to ATP and to ADP. The isopentenylated side chain is hydroxylated to form zeatin-type cytokinins. An alternative pathway, in which a hydroxylated side chain is directly added to the N6 position of the adenine moiety, has also been suggested.

Keywords

Arabidopsis AtIPTs Cytokinins DMAPP:ATP/ADP isopentenyltransferase Plant hormone 

Notes

Acknowledgments

I thank Thomas Moritz and Goran Sandberg for allowing me to cite unpublished data.

References

  1. Akiyoshi DE, Klee H, Amasino RM, Nester EW, Gordon MP (1984) T-DNA of Agrobacterium tumefaciens encodes an enzyme of cytokinin biosynthesis. Proc Natl Acad Sci USA 81:5994–5998PubMedGoogle Scholar
  2. Akiyoshi DE, Regier DA, Gordon MP (1987) Cytokinin production by Agrobacterium and Pseudomonas spp. J Bacteriol 169:4242–4248PubMedGoogle Scholar
  3. Akiyoshi DE, Regier DA, Gordon MP (1989) Nucleotide sequence of the tzs gene from Pseudomonas solanacearum strain K60. Nucleic Acids Res 17:88–86Google Scholar
  4. Armstrong DJ, Firtel RA (1989) Cytokinin oxidase activity in the cellular slime mold, Dictyostelium discoideum. Dev Biol 136:491–499PubMedGoogle Scholar
  5. Astot C, Dolezal K, Nordstrom A, Wang Q, Kunkel T, Moritz T, Chua NH, Sandberg G (2000) An alternative cytokinin biosynthesis pathway. Proc Natl Acad Sci USA 97:14778–14783CrossRefPubMedGoogle Scholar
  6. Barnes MF, Tien CL, Gray JS (1980) Biosynthesis of cytokinins by potato cell cultures. Phytochemistry 19:409–412CrossRefGoogle Scholar
  7. Barry GF, Rogers SG, Fraley RT, Brand L (1984) Identification of a cloned cytokinin biosynthetic gene. Proc Natl Acad Sci USA 81:4776–4780Google Scholar
  8. Beaty JS, Powell GK, Lica DA, Regier DA, MacDonald EMS, Hommes NG, Morris RO (1986) Tzs, a nopaline Ti plasmid gene from Agrobacterium tumefaciens associated with trans-zeatin biosynthesis. Mol Gen Genet 203:274–280Google Scholar
  9. Benkova E, Witters E, Van Dongen W, Kolar J, Motyka V, Brzobohaty B, Van Onckelen HA, Machackova I (1999) Cytokinins in tobacco and wheat chloroplasts: occurrence and changes due to light/dark treatment. Plant Physiol 121:245–252CrossRefPubMedGoogle Scholar
  10. Blackwell JR, Horgan R (1993) Cloned Agrobacterium tumefaciens ipt1 gene product, DMAPP:AMP isopentenyltransferase. Phytochemistry 34:1477–1481CrossRefGoogle Scholar
  11. Blackwell JR, Horgan R (1994) Cytokinin biosynthesis by extracts of Zea mays. Phytochemistry 35:339–342CrossRefGoogle Scholar
  12. Brown AC (1958) A physiological basis for the autonomous growth of the crown gall tumor cell. Proc Natl Acad Sci USA 44:344–349Google Scholar
  13. Chen C, Leisner S (1984) Modification of cytokinins by cauliflower microzomal enzymes. Plant Physiol 75:442-226Google Scholar
  14. Chen CM, Melitz DK (1979) Cytokinin biosynthesis in a cell-free system from cytokinin-autotrophic tobacco tissue cultures. FEBS Lett 107:15–20CrossRefPubMedGoogle Scholar
  15. Cherayil JD, Lipsett MN (1977) Zeatin ribonucleosides in the transfer ribonucleic acid of Rhizobium leguminosarum, Agrobacterium tumefaciens, Corynebacterium fascians, and Erwinia amylovora. J Bacteriol 131:741–744PubMedGoogle Scholar
  16. Crespi M, Messens E, Caplan AB, Van Montagu M, Desomer J (1992) Fasciation induction by the phytopathogen Rhodococcus fascians depends upon a linear plasmid encoding a cytokinin synthase gene. EMBO J 11:795–804PubMedGoogle Scholar
  17. Dewitte W, Chiappetta A, Azmi A, Witters E, Strnad M, Rembur J, Noin M, Chriqui D, Van Onckelen H (1999) Dynamics of cytokinins in apical shoot meristems of a day-neutral tobacco during floral transition and flower formation. Plant Physiol 119:111–122PubMedGoogle Scholar
  18. Emery RJ, Ma Q, Atkins CA (2000) The forms and sources of cytokinins in developing white lupine seeds and fruits. Plant Physiol 123:1593–1604CrossRefPubMedGoogle Scholar
  19. Faiss M, Zalubilova J, Strnad M, Schmülling T (1997) Conditional transgenic expression of the ipt gene indicates a function for cytokinins in paracrine signaling in whole tobacco plants. Plant J 12:401–415CrossRefPubMedGoogle Scholar
  20. Goethals K, Vereecke D, Jaziri M, Van Montagu M, Holsters M (2001) Leafy gall formation by Rhodococcus fascians. Annu Rev Phytopathol 39:27–52Google Scholar
  21. Golovko A, Sitbon F, Tillberg E, Nicander B (2002) Identification of a tRNA isopentenyltransferase gene from Arabidopsis thaliana. Plant Mol Biol 49:161–169CrossRefPubMedGoogle Scholar
  22. Goring H, Mardanov AA (1976) Influence of nitrogen deficiency on K/Ca ratio and cytokinin content of pumpkin seedlings. Biochem Physiol Pflanz 170:261–264Google Scholar
  23. Hardie DG, Carling D, Carlson M (1998) The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Annu Rev Biochem 67:821–855Google Scholar
  24. Hecht S, Eisenreich W, Adam P, Amslinger S, Kis K, Bacher A, Arigoni D, Rohdich F (2001) Studies on the nonmevalonate pathway to terpenes: the role of the GcpE (IspG) protein. Proc Natl Acad Sci USA 98:14837–14842CrossRefPubMedGoogle Scholar
  25. Horgan R (1984) Cytokinins. In: Wilkins MB (ed) Advanced plant physiology. Longmans, London, pp 89–101Google Scholar
  26. Houba-Herin N, Pethe C, d'Alayer J, Laloue M (1999) Cytokinin oxidase from Zea mays: purification, cDNA cloning and expression in moss protoplasts. Plant J 17:615–626PubMedGoogle Scholar
  27. Jacqmard A, Detry N, Dewitte W, Van Onckelen H, Bernier G (2002) In situ localisation of cytokinins in the shoot apical meristem of Sinapis alba at floral transition. Planta 214:970–973CrossRefPubMedGoogle Scholar
  28. Kakimoto T (2001) Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. Plant Cell Physiol 42:677–685Google Scholar
  29. Krall L, Raschke M, Zenk MH, Baron C (2002) The Tzs protein from Agrobacterium tumefaciens C58 produces zeatin riboside 5′-phosphate from 4-hydroxy-3-methyl-2-(E)-butenyl diphosphate and AMP. FEBS Lett 527:315–318CrossRefPubMedGoogle Scholar
  30. Laloue M, Terrine C, Gawer M (1974) Cytokinins: formation of the nucleoside-5′-tri phosphate in Tobacco and Acer cells. FEBS Lett 46:45–50CrossRefPubMedGoogle Scholar
  31. Letham DS (1994) Cytokinins as phytohormones: sites of biosynthesis, translocation, and function of translocated cytokinin. CRC, Boca RatonGoogle Scholar
  32. Lichter A, Barash I, Valinsky L, Manulis S (1995) The genes involved in cytokinin biosynthesis in Erwinia herbicola pv. gypsophilae: characterization and role in gall formation. J Bacteriol 177:4457–4465PubMedGoogle Scholar
  33. McKenzie MJ, Mett VV, Stewart Reynolds PH, Jameson PE (1998) Controlled cytokinin production in transgenic tobacco using a copper-inducible promoter. Plant Physiol 116:969–977CrossRefPubMedGoogle Scholar
  34. Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118Google Scholar
  35. Morris RO, Blevins DG, Dietrich JT, Durley RC, Gelvin SB, Gray J, Hommes NG, Kaminek M, Mathesius U, Meilan R, Reinbott TM, Sayavedra-Soto L (1993) Cytokinins in plant pathogenic bacteria and developing cereal grains. Aust J Plant Physiol 20:621–637Google Scholar
  36. Morris RO, Bilyeu KD, Laskey JG, Cheikh NN (1999) Isolation of a gene encoding a glycosylated cytokinin oxidase from maize. Biochem Biophys Res Commun 255:328–333PubMedGoogle Scholar
  37. Nomura T, Tanaka Y (1977) Cytokinin activity of discadenine: a spore germination inhibitor of Dictyostelium discoideum. Phytochemistry 16:1819–1820CrossRefGoogle Scholar
  38. Powell GK, Morris RO (1986) Nucleotide sequence and expression of a Pseudomonas savastanoi cytokinin biosynthetic gene: homology with Agrobacterium tumefaciens tmr and tzs loci. Nucleic Acids Res 14:2555–2565Google Scholar
  39. Redig P, Schmülling T, Van Onckelen H (1996a) Analysis of cytokinin metabolism in ipt transgenic tobacco by liquid chromatography-tandem mass spectrometry. Plant Physiol 112:141–148PubMedGoogle Scholar
  40. Redig P, Shaul O, Inze D, Van Montagu M, Van Onckelen H (1996b) Levels of endogenous cytokinins, indole-3-acetic acid and abscisic acid during the cell cycle of synchronized tobacco BY-2 cells. FEBS Lett 391:175–180PubMedGoogle Scholar
  41. Rohdich F, Kis K, Bacher A, Eisenreich W (2001) The non-mevalonate pathway of isoprenoids: genes, enzymes and intermediates. Curr Opin Chem Biol 5:535–540CrossRefPubMedGoogle Scholar
  42. Sakakibara H, Takei K (2002) Identification of cytokinin biosynthesis genes in Arabidopsis: a breakthrough for understanding the metabolic pathway and the regulation in higher plants. J Plant Growth Regul 21:17–23CrossRefPubMedGoogle Scholar
  43. Salama AM, Wareing PF (1979) Effects of mineral nutrition on endogenous cytokinins in plants of sunflower. J Exp Bot 30:971–981Google Scholar
  44. Samuelson ME, Larsson C-M (1993) Nitrate regulation of zeatin riboside levels in barley roots: effects of inhibitors of N assimilation and comparison with ammonium. Plant Sci 93:77–84CrossRefGoogle Scholar
  45. Skoog F, Armstrong DJ (1970) Cytokinins. Annu Rev Plant Physiol 21:359–384Google Scholar
  46. Sun J, Niu QW, Tarkowski P, Zheng B, Tarkowska D, Sandberg G, Chua NH, Zuo J (2003) The Arabidopsis AtIPT8/PGA22 gene encodes an isopentenyl transferase that is involved in de novo cytokinin biosynthesis. Plant Physiol 131:167–176CrossRefPubMedGoogle Scholar
  47. Takei K, Sakakibara H, Sugiyama T (2001a) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J Biol Chem 276:26405–26410CrossRefPubMedGoogle Scholar
  48. Takei K, Sakakibara H, Taniguchi M, Sugiyama T (2001b) Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol 42:85–93Google Scholar
  49. Takei K, Takahashi T, Sugiyama T, Yamaya T, Sakakibara H (2002) Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. J Exp Bot 53:971–977CrossRefPubMedGoogle Scholar
  50. Taya Y, Tanaka Y, Nishimura S (1978) 5′-AMP is a direct precursor of cytokinin in Dictyostelium discoideum. Nature 271:545–547PubMedGoogle Scholar
  51. Yamada H, Suzuki T, Terada K, Takei K, Ishikawa K, Miwa K, Yamashino T, Mizuno T (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42:1017–1023Google Scholar
  52. Yang J, Zhang J, Wang Z, Zhu Q, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127:315–323PubMedGoogle Scholar
  53. Zubko E, Adams CJ, Machaekova I, Malbeck J, Scollan C, Meyer P (2002) Activation tagging identifies a gene from Petunia hybrida responsible for the production of active cytokinins in plants. Plant J 29:797–808CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer-Verlag  2003

Authors and Affiliations

  1. 1.Department of Biology, Graduate School of ScienceOsaka UniversityToyonakaJapan
  2. 2.Precursory Research for Embryonic Science and Technology (PRESTO)Science and Technology CorporationKawaguchiJapan

Personalised recommendations