Plant Molecular Biology

, Volume 67, Issue 3, pp 295–304 | Cite as

Helitron mediated amplification of cytochrome P450 monooxygenase gene in maize

  • Natalie Jameson
  • Nikolaos Georgelis
  • Eric Fouladbash
  • Sara Martens
  • L. Curtis Hannah
  • Shailesh LalEmail author


The mass movement of gene sequences by Helitrons has significantly contributed to the lack of gene collinearity reported between different maize inbred lines. However, Helitron captured-genes reported to date represent truncated versions of their progenitor genes. In this report, we provide evidence that maize CYP72A27-Zm gene represents a cytochrome P450 monooxygenase (P450) gene recently captured by a Helitron and transposed into an Opie-2 retroposon. The four exons of the CYP72A27 gene contained within the element contain a putative open reading frame (ORF) for 428 amino acid residues. We provide evidence that Helitron captured CYP72A27-Zm is transcribed. To identify the progenitor gene and the evolutionary time of capture, we searched the plant genome database and discovered other closely related CYP72A27-Zm genes in maize and grasses. Our analysis indicates that CYP72A27-Zm represents an almost complete copy of maize CYP72A26-Zm gene captured by a Helitron about 3.1 million years ago (mya). The Helitron-captured gene then duplicated twice, approximately 1.5–1.6 mya giving rise to CYP72A36-Zm and CYP72A37-Zm. These data provide evidence that Helitrons can capture and mobilize intact genes that are transcribed and potentially encode biologically relevant proteins.


Gene capture Genome evolution Helitrons Transposable elements 



This work immensely benefited from maize CYP72A26 and CYP72A27 genes deposited in GenBank by Dr. Mary Schuler’s group, University of Illinois. We thank Dr. Schuler for her kind help and suggestions during the course of this project. The work was supported by National Science Foundation (USA) grant 0514759 to SL.


  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  2. Bennetzen JM (2005) Transposable elements, gene creation and genome rearrangement in flowering plants. Curr Opin Genet Dev 15:1–7CrossRefGoogle Scholar
  3. Brunner S, Pea G, Rafalski A (2005) Origins, genetic organization and transcription of a family of non-autonomous Helitron elements in maize. Plant J 43:799–810PubMedCrossRefGoogle Scholar
  4. Curcio MJ, Derbyshire KM (2003) The outs and ins of transposition: from mu to kangaroo. Nat Rev Mol Cell Biol 4:865–877CrossRefGoogle Scholar
  5. Dooner HK, Lal SK, Hannah LC (2006) Suggested guidelines for naming Helitrons. Maize Genetics Coop Newslet 81, Scholar
  6. Elrouby N, Bureau TE (2001) A novel hybrid open reading frame formed by multiple cellular gene transductions by a plant long terminal repeat retroelement. J Biol Chem 276:41963–41968PubMedCrossRefGoogle Scholar
  7. Feschotte C, Wessler SR (2001) Treasures in the attic: Rolling circle transposons discovered in eucaryotic genomes. Proc Natl Acad Sci USA 98:8923–8924PubMedCrossRefGoogle Scholar
  8. Feschotte C, Jiang N, Wessler SR (2003) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329–341CrossRefGoogle Scholar
  9. Fu H, Dooner HK (2002) Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci USA 99:9573–9578PubMedGoogle Scholar
  10. Gaut BS, Morton BR, McCaig BC, Clegg MT (1996) Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci USA 93:10274–10279PubMedCrossRefGoogle Scholar
  11. Gu X, Fu YX, Li WH (1995) Maximum likelihood estimation of the heterogeneity of substitution rate among nucleotide sites. Mol Biol Evol 12:546–557PubMedGoogle Scholar
  12. Gupta S, Gallavotti A, Stryker GA, Schmidt RJ, Lal SK (2005) A novel class of Helitron-related transposable elements in maize contain portions of multiple cellular genes. Plant Mol Biol 57:115–127PubMedCrossRefGoogle Scholar
  13. Jiang N, Bao ZR, Zhang XY, Eddy SR, Wessler SR (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573PubMedCrossRefGoogle Scholar
  14. Jin Y-K, Bennetzen JL (1994) Integration and nonrandom mutation of a plasma membrane proton ATPase gene fragment within the Bs1 retroelement of maize. Plant Cell 6:1177–1186PubMedCrossRefGoogle Scholar
  15. Kapitonov VV, Jurka J (2001) Rolling circle transposons in eukaryotes. Proc Natl Acad Sci USA 17:8714–8719CrossRefGoogle Scholar
  16. Kapitonov VV, Jurka J (2003) Molecular paleontology of transposable elements in the Drosophila melanogaster genome. Proc Natl Acad Sci USA 11:6569–6574CrossRefGoogle Scholar
  17. Kawasaki S, Nitasaka E (2004) Characterization of Tpn1 family in the Japanese morning glory: En/Spm-related transposable elements capturing host genes. Plant Cell Physiol 45:933–944PubMedCrossRefGoogle Scholar
  18. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  19. Kumar S, Tamura K, Nei N (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  20. Lai J, Li Y, Messing J, Dooner HK (2005) Gene movement by Helitron transposons contributes to the haplotype variability of maize. Proc Natl Acad Sci USA 102:9068–9073PubMedCrossRefGoogle Scholar
  21. Lal SK, Hannah LC (2005a) Helitrons contribute to the lack of gene colinearity observed in modern maize inbreds. Proc Natl Acad Sci USA 102:9993–9994PubMedCrossRefGoogle Scholar
  22. Lal SK, Hannah LC (2005b) Massive changes of the maize genome are caused by Helitrons. Heredity 95:421–422PubMedCrossRefGoogle Scholar
  23. Lal SK, Giroux MJ, Brendel V, Vallejos E, Hannah LC (2003) The maize genome contains a Helitron insertion. Plant Cell 15:381–391PubMedCrossRefGoogle Scholar
  24. Lal SK, Georgelis N, Hannah LC (2008) Helitrons: their impact on maize genome evolution and diversity. In: Hake S, Bennetzen JL (eds) The maize handbook: domestication, genetics, and genome (in press)Google Scholar
  25. Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A, 2005 Gene duplication and exon shuffling by Helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37:997–1002PubMedCrossRefGoogle Scholar
  26. Poulter RT, Goodwin TJ, Butler MI (2003) Vertebrate helentrons and other novel Helitrons. Gene 313:201–212PubMedCrossRefGoogle Scholar
  27. Pritham EJ, Feschotte C (2007) Massive amplification of rolling-circle transposons in the lineage of the bat Myotis Lucifugus. Proc Natl Acad Sci USA 104:1895–1900PubMedCrossRefGoogle Scholar
  28. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons in maize. Nat Genet 20:43–45PubMedCrossRefGoogle Scholar
  29. SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposon in the intergenic regions of the maize genome. Science 274:765–768PubMedCrossRefGoogle Scholar
  30. Schuler MA, Werck-Reichhart D (2003) Functional genomics of P450s. Ann Rev Plant Biol 54:629–667CrossRefGoogle Scholar
  31. Song R, Messing J (2003) Gene expression of a gene family in maize based on noncollinear haplotypes. Proc Natl Acad Sci USA 100:9055–9060PubMedCrossRefGoogle Scholar
  32. Talbert LE, Chandler VL (1988) Characterization of a highly conserved sequence related to mutator transposable elements in maize . Mol Biol Evol 5:519–529PubMedGoogle Scholar
  33. Usuka J, Brendel V (2000) Gene structure prediction by spliced alignment of genomic DNA with protein sequences: increased accuracy by differential splice site scoring. J Mol Biol 297:1075–1085PubMedCrossRefGoogle Scholar
  34. Usuka J, Zhu W, Brendel V (2000) Optimal spliced alignment of homologous cDNA to a genomic DNA template. Bioinformatics 16:203–211PubMedCrossRefGoogle Scholar
  35. Vale RD, Flettereick RJ (1997) The design plan of kinesin motors. Annu Rev Cell Dev Biol 13:745–777PubMedCrossRefGoogle Scholar
  36. Xu JH, Messing J (2006) Maize haplotype with a Helitron-amplified cytodine deaminase gene copy. BMC Genet 7:52PubMedCrossRefGoogle Scholar
  37. Yang Z (1994) Estimating the pattern of nucleotide substitution. J Mol Evol 39:105–111PubMedGoogle Scholar
  38. Zhang Z, Gerstein M (2004) Large scale analysis of pseudogenes in the human genome. Curr Opin Genet Dev 14:328–335PubMedCrossRefGoogle Scholar
  39. Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. Dissertation, The University of Texas at AustinGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Natalie Jameson
    • 1
  • Nikolaos Georgelis
    • 2
  • Eric Fouladbash
    • 1
  • Sara Martens
    • 1
  • L. Curtis Hannah
    • 2
  • Shailesh Lal
    • 1
    Email author
  1. 1.Department of Biological SciencesOakland UniversityRochesterUSA
  2. 2.Department of Horticultural Sciences and Program in Plant Molecular and Cellular BiologyUniversity of FloridaGainesvilleUSA

Personalised recommendations