Molecular and General Genetics MGG

, Volume 246, Issue 1, pp 100–109 | Cite as

Expression of a cytochrome P450 gene family in maize

  • Monika Frey
  • Ralf Kliem
  • Heinz Saedler
  • Alfons Gierl
Original Paper

Abstract

Maize seedlings, like seedlings of many other plants, are rich in cytochrome P450 (P450) enzyme activity. Four P450 genes (CYPzm1–4), isolated from a seedling-specific cDNA library, are characterised by a transient and seedling-specific expression pattern. The maximum steady state mRNA levels are reached at 3 days in root and at 7 days in shoot tissue, respectively. All four genes belong to one gene family and are closely related to the CYP71 family of plant P450 genes, which includes the enzymes of the ripening avocado fruit (CYP71A1) and eggplant hypocotyls (CYP71A2, A3, A4). The expression of these related P450 genes in monocot and dicot plants indicates that these enzymes play a significant role in plants; however, the in vivo enzyme functions are unknown. The divergence of the four members of the maize gene family is sufficiently high to account for different substrate and/or reaction specificity. Although the general expression pattern of the four genes is identical, the maximum steady-state mRNA levels vary in different maize lines. In situ hybridisation reveals the highest mRNA levels in the coleoptile, the first developed leaflets, the ground tissue of the nodular complex, and in the cortex and pith of the region of cell division in the root. The mapping of the maize CYPzm genes shows that, as in animals, P450 genes of the same family can be clustered. The presence of the CYPzm gene cluster in maize argues for generation of distinct plant P450 gene families by gene duplication.

Key words

Cytochrome P450 Gene family Maize seedling Gene organisation Expression pattern 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bailey BA, Larson RL (1991) Maize microsomal benzoxazinone N-monooxygenase. Plant Physiol 95:792–796Google Scholar
  2. Bozak K, Yu H, Sirevåg R, Christoffersen RE (1990) Sequence analysis of ripening related cytochrome P-450 cDNAs from avocado fruit. Proc Natl Acad Sci USA 87:3904–3908Google Scholar
  3. Bozak KR, O'Keefe DP, Christoffersen RE (1992) Expression of a ripening-related avocado (Persea americana) cytochrome P450 in yeast. Plant Physiol 100:1976–1981Google Scholar
  4. Burr B, Burr FA (1991) Recombinant inbreds for molecular mapping in maize: theoretical and practical considerations. Trends Genet 7:55–60Google Scholar
  5. Butt VS, Lamb CJ (1981) Oxygenases and the metabolism of plant products. In: Conn EE (ed) The biochemistry of plants, vol. 7. Academic Press, New York, pp 627–665Google Scholar
  6. Donaldson RP, Luster DG (1991) Multiple forms of plant cytochromes P-450. Plant Physiol 96:669–674Google Scholar
  7. Fahrendorf T, Dixon RA (1993) Stress responses in Alfalfa (Medicago sativa L.). XVIII: Molecular cloning and expression of the elicitor-inducible cinnamic acid 4-hydroxylase cytochrome P450. Arch Biochem Biophys 305:509–515Google Scholar
  8. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791Google Scholar
  9. Feng D-F, Doolittle RF (1987) Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J Mol Evol 2:351–360Google Scholar
  10. Frey M, Reinecke J, Grant S, Saedler H, Gierl A (1990) Excision of the En/Spm transposable element of Zea mays requires two element-encoded proteins. EMBO J 9:4037–4044Google Scholar
  11. Gonzales FJ, Nebert DW (1990) Evolution of the P450 gene superfamily: animal-plant ‘warfare’, molecular drive, and human genetic differences in drug oxidation. Trends Genet 6:182–186Google Scholar
  12. Hamilton RH (1964) A corn mutant deficient in 2,4-dihydroxy-7methoxy-1,4-benzoxazin-3-one with an altered tolerance of atrazine. Weeds 12:27–30Google Scholar
  13. Higashi YU, Yoshioka H, Yamane M, Gotoh O, Fuji-Kurijama Y (1986) Complete nucleotide sequence of the two steroid 21-hydroxylase genes tandemly arranged in the human chromosome: a pseudogene and a genuine one. Proc Natl Acad Sci USA 83:2841–2845Google Scholar
  14. Holton TA, Brugliera F, Lester DR, Tanaka Y, Hyland CD, Menting JG, Lu C-Y, Farcy E, Stevenson TN, Cornish EC (1993) Cloning and expression of cytochrome P450 genes controlling flower colour. Nature 366:276–279Google Scholar
  15. Huijser P, Klein J, Lonning W-E, Meijer H, Saedler H, Sommer H (1992) Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO J 11:1239–1249Google Scholar
  16. Kalb VF, Loper JC (1988) Proteins from eight eucaryotic cytochrome P450 families share a segmented region of sequence similarity. Proc Natl Acad Sci USA 85:7221–7225Google Scholar
  17. Larson RL, Bussard JB (1986) Microsomal flavonoid 3′-monooxygenase from maize seedlings. Plant Physiol 80:483–486Google Scholar
  18. Mangold U, Eichel J, Batschauer A, Lanz T, Kaiser T, Spangenberg G, Werck-Reichhart D, Schröder J (1994) Gene and cDNA for plant cytochrome P450 proteins (CYP72 family) from Catharanthus roseus, and transgenic expression of a gene and cDNA in tobacco and Arabidopsis thaliana. Plant Sci 96:129–136Google Scholar
  19. Matsunaga T, Umeno M, Gonzales FJ (1990) The rat P450 IID subfamily, complete sequences of four closely linked genes and evidence that gene conversion maintained sequence homogeneity at the heme-binding region of the cytochrome P450 active site. J Mol Evol 30:155–169Google Scholar
  20. Menssen A, Höhmann S, Martin W, Schnable PS, Peterson PA, Saedler H, Gierl A (1990) The En/Spm transposable element of Zea mays contains splice sites at the termini generating a novel intron from a dSpm element in the A2 gene. EMBO J 9:3051–3057Google Scholar
  21. Mizutani M, Ward E, DiMaio J, Otha D, Ryals J, Sato R (1993) Molecular cloning and sequence of a cDNA encoding mung bean cytochrome P450 (P450Ch4) possessing cinnamate 4-hydroxylase activity. Biochem Biophys Res Commun 190:875–880Google Scholar
  22. Nebert DR, Strobel HW (1987) Evolution of cytochrome P450 proteins. Mol Biol Evol 46:572–593Google Scholar
  23. Nebert DW, Nelson DR, Coon MJ, Estabrook RW, Feyereisen R, Fujii-Kuriyama Y, Gonzalez FJ, Guengerich FP, Gunsalus IC, Johnson EF, Loper JC, Sato R, Waterman MR, Waxman DJ (1991) The P450 superfamily: update on new sequences, gene mapping and recommended nomenclature. DNA Cell Biol 10:1–14Google Scholar
  24. Niemeyer HM (1988) Hydroxamic acids (4-hydroxy-1,4-benzoxazin-3-ones), defence chemicals in the Gramineae. Phytochemistry 27:3349–3358Google Scholar
  25. Picado-Leonard J, Miller WL (1987) Cloning and sequence of the human gene for P450c17 (steroid 17a-hydroxylase/17/20lyase): similarity with the gene for P450c21. DNA 6:439–448Google Scholar
  26. Simcox KD, Weber DF (1985) Location of the benzoxazinless (bx) locus in maize by monosomic and B-A translocation analysis. Crop Sci 25:827–830Google Scholar
  27. Sommer H, Beltrán J-P, Huijser P, Pape H, Lönning W-E, Saedler H, Schwarz-Sommer Zs (1990) Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus, the protein shows homology to transcription factors. EMBO 19:605–613Google Scholar
  28. Teutsch HG, Hasenfratz MP, Lesot A, Stoltz C, Garnier J-M, Jeltsch J-M, Durst F, Werck-Reichhart D (1993) Isolation and sequence of a cDNA encoding the Jerusalem artichoke cinnamate 4-hydroxylase, a major plant cytochrome P450 involved in the general phenylpropanoid pathway. Proc Natl Acad Sci USA 90:4102–4106Google Scholar
  29. Toguri T, Kobayashi O, Umemoto, N (1993a) The cloning of eggplant seedling cDNAs encoding proteins from a novel cytochrome P-450 family (CYP76). Biochem Biophys Acta 1216:165–169Google Scholar
  30. Toguri T, Umemoto N, Kobayashi O, Ohtani T (1993b) Activation of anthocyanin synthesis genes by white light in eggplant hypocotyl tissues, and identification of an inducible P-450 cDNA. Plant Mol Biol 23:933–946Google Scholar
  31. Umemoto, N, Kobayashi O, Ishizaki-Nishizawa O, Toguri T (1993) cDNAs sequences encoding cytochrome P450 (CYP71 family) from eggplant seedlings. FEBS Lett 12957:169–173Google Scholar
  32. Vetter H-P, Mangold U, Schröder G, Marner F-J, Werck-Reichhart D, Schröder J (1992) Molecular analysis and heterologous expression of an inducible cytochrome P-450 protein from periwinkle (Catharanthus roseus L.) Plant Physiol 100:998–1007Google Scholar
  33. West CA (1980) Hydroxylases, mono-oxygenases and cytochrome P-450. In: Davis DD (ed) The biochemistry of plants, vol 2. Academic Press, New York, pp 317–364Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Monika Frey
    • 1
  • Ralf Kliem
    • 1
  • Heinz Saedler
    • 1
  • Alfons Gierl
    • 1
  1. 1.Max-Planck-Institut für ZüchtungsforschungAbteilung Molekulare PflanzengenetikKölnGermany

Personalised recommendations