Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

PREM-2, a copia-type retroelement in maize is expressed preferentially in early microspores

Abstract

We have isolated, by screening a genomic library, a retroelement from maize designated PREM-2 (pollen retroelement maize-2), which is expressed in a tissue-specific manner. RNA transcripts of the PREM-2 family are found in the microspore but not in more mature pollen or in any of the vegetative tissues examined. The expression of PREM-2 elements in the uninucleate microspore provides an explanation for the genetic transmission of genomic rearrangements caused by the transposition of retroelements. PREM-2 elements are very abundant and are estimated to constitute about 5% of the maize genome and could possibly have played an important role in the determination of genome structure and in the generation of repetitive sequences in maize. The entire PREM-2 element is 9439 by long. The LTRs of PREM-2 are 1307 by in length. The internal region between the 5′ and 3′ LTRs contains 6825 by and shares homology to the gag, pro, int, RT, and RNaseH regions of copia-type retroelements. PREM-2 elements have been found in close proximity with several maize genes registered in GenBank. The presence of PREM-2 sequence in the exact 5' flanking position of three polygalacturonase genes expressed in pollen, has been used to examine the evolution of the polygalacturonase multigene family in maize and to estimate the time of the PREM-2 integration event.

This is a preview of subscription content, log in to check access.

References

  1. Allen RL, Lonsdale DM (1993) Molecular characterization of one of the maize polygalacturonase gene family members which are expressed during late pollen development. Plant J 3:261–271

  2. Barakate A, Martin W, Quigley F, Mache R (1993) Characterization of a multigene family encoding an exopolygalacturonase in maize. J Mol Biol 229:797–801

  3. Barciszewska MZ, Joachimiak A, Barciszewski J (1989) The initiator transfer ribonucleic acid from yellow lupin seeds, correction of nucleotide sequence and crystallization. Phytochemistry 28:2039–2043

  4. Berlani RE, Walbot V, Davis RW (1988) Sequence analysis of three fragments of maize nuclear DNA which replicate autonomously in yeast. Plant Mol Biol 11:173–182

  5. Boeke JD, Corces VG (1989) Transcription and reverse transcription of retrotransposons. Ann Rev Microbiol 43:403–434

  6. Bureau TE, Wessler SR (1992)Tourist: a large family of sall inverted repeat elements frequently associated with maize genes. Plant Cell 4:1283–1294

  7. Bureau TE, White SE, Wessler SR (1994) Transduction of a cellular gene by a plant retroelement. Cell 77:479–480

  8. Camirand A, St-Pierre B, Marineau C, Brisson N (1990) Occurrence of a copia-like transposable element in one of the introns of the potato starch phosphorylase gene. Mol Gen Genet 224:33–39

  9. Casacuberta JM, Grandbastien M-A (1993) Characterization of LTR sequences involved in the protoplast specific expression of the tobacco Tntl retrotransposon. Nucl Acids Res 21:2087–2093

  10. Chalker DL, Sandmeye SB (1992) Ty3 integrates within the region of RNA polymerase III transcription initiation. Gene Develop 6:117–128

  11. Dellaporta SL, Wood J, Hicks JB (1985) Maize DNA miniprep. In: Malmberg R, Messing J, Sussex I (eds) Molecular biology of plants: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 36–37

  12. Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603

  13. Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13

  14. Felsenstein J (1993) PHYLIP (Phylogenetic Inference Package), version 3.5. Computer software and manual distributed by the author, Department of Genetics, University of Washington, Seattle, Wash

  15. Flavell AJ (1992)Tyl-copia group retrotransposons and the evolution of retroelements in the eukaryotes. Genetica 86:203–214

  16. Flavell RB (1986) Repetitive DNA and chromosome evolution in plants. Philos Trans R Soc London Set B 312:227–242

  17. Ghosh HP, Ghosh K, Simsek M, RajBhandary UL (1982) Nucleotide sequence of wheat germ cytoplasmic initiator methionine transfer ribonucleic acid. Nucleic Acids Res 10:3241–3247

  18. Grandbastien M-A (1992) Retroelements in higher plants. Trends Genet 8:103–108

  19. Grandbastien M-A, Spielmann A, Caboche M (1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337:376–380

  20. Hamilton DA, Bashe DM, Stinson JR, Mascarenhas JP (1989) Characterization of a pollen-specific genomic clone from maize. Sex Plant Reprod 2:208–212

  21. Hamilton DA, Mascarenhas JP (1996) Gene expression during pollen development. In: Sawhney VK, Shivanna KR (eds) Pollen biotechnology for crop production and improvement. Cambridge University Press (in press)

  22. Hirochika H (1993) Activation of tobacco retrotransposons during tissue culture. EMBO J 12:2521–2528

  23. Ji H, Moore DP, Blomberg MA, Braiterman LT, Voytas DF, Natsoulis G, Boeke JD (1993) Hotspots for unselected Tyl transposition events on yeast chromosome III are near tRNA genes. Cell 73:1007–1018

  24. Jin Y-K, Bennetzen JL (1989) Structure and coding properties ofBs1, a maize retrovirus-like transposon. Proc Natl Acad Sci USA: 86:6235–6239

  25. Jin YK, Bennetzen JL (1994) Integration and nonrandom mutation of a plasma membrane proton ATPase gene fragment within theBs1 retroelement of maize. Plant Cell 6:1177–1186

  26. Joshi CP (1987) An inspection of the domain between putative TATA box and translation start site in 79 plant genes. Nucleic Acids Res 15:6643–6653

  27. Konieczny A, Voytas DF, Cummings MP, Ausubel FM (1991) A superfamily ofArabidopsis thaliana retrotransposons. Genetics 127:801–809

  28. Leeton PRJ, Smyth DR (1993) An abundant LINE-like element amplifed in the genome ofLilium speciosum. Mol Gen Genet 237:97–104

  29. Lewin B (1994) Genes V. Oxford University Press, Oxford

  30. Li W-H, Wu C-I, Luo C-C. (1985) A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative liklihood of nucleotide substitution and codon changes. Mol Biol Evol 2:150–174

  31. Manninen I, Schulman AH (1993)BARE-1, acopia-like retroelement in barley (Hordeum vulgare L). Plant Mol Biol 22:829–846

  32. Mascarenhas JP, Turcich MP (1994) The activity of retroelements during male gametophyte development. In: Kao T-h, Stephenson AG (eds) Pollen-pistil interactions and pollen tube growth. American Society of Plant Physiologists, Rockville, Md, pp 39–44

  33. McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

  34. McDonald JF (1990) Macroevolution and retroviral elements. BioScience 40:183–191

  35. Mulcahy DL, Mulcahy GB (1987) The effects of pollen competition. Am Sci 75:44–50

  36. Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607

  37. Palmgren MG (1994) Capturing of host DNA by a plant retroelement — Bs1 encodes plasma membrane H+-ATPase domains. Plant Mol Biol 25:137–140

  38. Pouteau S, Huttner E, Grandbastien MA, Caboche M (1991) Specific expression of the tobacco Tntlretrotransposon in protoplasts. EMBO J 10:1911–1918

  39. Pouteau S, Grandbastien M-A, Boccara M (1994) Microbial elicitors of plant defense responses activate transcription of a retrotransposon. Plant J 5:535–542

  40. Purugganan MD, Wessler SR (1994) Molecular evolution ofmagellan, a maize Ty3/gypsy-like retrotransposon. Proc Natl Acad Sci USA 91:11674–11678

  41. Quigley F, Martin WF, Cerff R (1988) Intron conservation across the prokaryote-eukaryote boundary: structure of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize. Proc Natl Acad Sci USA 85:2672–2676

  42. Robins DM, Samuelson LC (1992) Retrotransposons and the evolution of mammalian gene expression. Genetica 86:191–201

  43. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

  44. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

  45. Schwarz-Sommer Z, Leclercq L, Gobel E, Saedler H (1987) Cin4, an insert altering the structure of theA1 gene inZea mays, exhibits properties of nonviral retrotransposons. EMBO J 6:3873–3880

  46. Shepherd NS, Schwarz-Sommer Z, Blumberg vel Spalve J, Gupta M, Wienand U, Saedler H (1984) Similarity of the Cin1 repetitive family ofZea mays to eukaryotic transposable elements. Nature 307:185–187

  47. Smith PA, Corces VG (1991) Drosophila transposable elements: mechanisims of mutagenesis and interactions with the host genome. Adv Genet 29:229–300

  48. Smyth DR, Kalitsis P, Joseph JL, Sentry JW (1989) Plant retrotransposon fromLilium henri is related toTy3 of yeast and the gypsy group ofDrosophila. Proc Natl Acad Sci USA 86:5015–5019

  49. Stinson JR, Eisenberg AJ, Willing RP, Pe ME, Hanson DD, Mascarenhas JP (1987) Genes expressed in the male gametophyte of flowering plants and their isolation. Plant Physiol 83:442–447

  50. Swofford DL (1993) PAUP: phylogenetic analysis using parsimony, version 3.1. Computer program distributed by Illinois Natural History Survey, Champaign, Ill

  51. Turcich MP, Mascarenhas JP (1994) PREM-1, a putative maize retroelement has LTR (long terminal repeat) sequences that are preferentially transcribed in pollen. Sex Plant Reprod 7:2–11

  52. Varagona MJ, Purugganan M, Wessler SR (1992) Alternative splicing induced by insertion of retrotransposons into the maizewaxy gene. Plant Cell 4:811–820

  53. Voytas DF, Boeke JD (1993) Yeast retrotransposons and tRNAs. Trends Genet 9:421–427

  54. Voytas DF, Cummings MP, Konieczny A, Ausubel FM, Rodermel SR (1992) copia-like retrotransposons are ubiquitous among plants. Proc Natl Acad Sci USA 89:7124–7128

  55. Weil CF, Wessler SR (1990) The effects of plant transposable element insertion on transcription initiation and RNA processing. Annu Rev Plant Physiol 41:527–552

  56. Weiner AM, Deininger PL, Efstratiadis A (1986) Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Ann Rev Biochem 55:631–661

  57. White SE, Habera LF, Wessler SR (1994) Retrotransposons in the flanking regions of normal genes: a role for copia-like elements in the evolution of gene structure and expression. Proc Natl Acad Sci USA 91:11792–11796

  58. Willing RP, Mascarenhas JP (1984) Analysis of the complexity and diversity of mRNAs from pollen and shoots ofTradescantia. Plant Physiol 75:865–868

  59. Wolfe KH, Sharp PM, Li W-H (1989) Rates of synonymous substitution in plant nuclear genes. J Mol Evol 29:208–211

Download references

Author information

Correspondence to J. P. Mascarenhas.

Additional information

The nucleotide sequence data reported appear in the Genebank, EMBL and DDBJ databases under the accession numbers U41000, U41079 and U41080.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Turcich, M.P., Bokhari-Riza, A., Hamilton, D.A. et al. PREM-2, a copia-type retroelement in maize is expressed preferentially in early microspores. Sexual Plant Reprod 9, 65–74 (1996). https://doi.org/10.1007/BF02153053

Download citation

Key words

  • Maize
  • Retrotransposon
  • Microspore expression
  • Polygalacturonase genes
  • Genome structure