Abstract
The transposon Mutator was first identified in maize, and is one of the most active mobile elements in plants. The Arabidopsis thaliana genome contains at least 200 Mutator-like elements (MULEs), which contain the Mutator-like transposase gene, and often additional genes. We have detected a novel type of MULEs in melon (CUMULE), which, besides the transposase, contains two ubiquitin-like specific protease-like sequences (ULP1). This element is not present in the observed location in some melon cultivars. Multiple copies of this element exist in the Cucumis melo genome, and it has been detected in other Cucurbitaceae species. Analysis of the A. thaliana genome revealed more than 90 CUMULE-like elements, containing one or two Ulp1-like sequences, although no evidence of mobility exists for these elements. We detected various putative transposable elements containing ULP1-like sequences in rice. The discovery of these MULEs in melon and Arabidopsis, and the existence of similar elements in rice and maize, suggest that a proteolytic function may be important for this subset of the MULE transposable elements.
Similar content being viewed by others
References
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–218
Balakirev MY, Jaquinod M, Haas AL, Chroboczek J (2002) Deubiquitinating function of adenovirus proteinase. J Virol 76:6323–6331
Barrett AJ, Rawlings ND (2001) Evolutionary lines of cysteine peptidases. Biol Chem 382:727–733
Bennetzen JL (1996) The Mutator transposable element system of maize. Curr Top Microbiol Immunol 204:195–229
Brodie R, Roper RL, Upton C (2004) JDotter: a Java interface to multiple dotplots generated by dotter. Bioinformatics 20:279–281
Felsenstein J (1989) PHYLIP—Phylogeny Inference Package (Version 3.2). Cladistics 5:164–166
Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle
Hoen DR, Park KC, Elrouby N, Yu Z, Mohabir N, Cowan RK, Bureau TE (2006) Transposon-mediated expansion and diversification of a family of ULP-like genes. Mol Biol Evol 23:1254–1268
Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573
Juretic N, Hoen DR, Huynh ML, Harrison PM, Bureau TE (2005) The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Res 15:1292–1297
Jones JM, Welty DJ, Nakai H (1998) Versatile action of Escherichia coli ClpXP as protease or molecular chaperone for bacteriophage Mu transposition. J Biol Chem 273:459–465
Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung DY, Vierstra RD (2003) The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. J Biol Chem 278:6862–6872
Le QH, Wright S, Yu Z, Bureau T (2000) Transposon diversity in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:7376–7381
Lisch D, Girard L, Donlin M, Freeling M (1999) Functional analysis of deletion derivatives of the maize transposon MuDR delineates roles for the MURA and MURB proteins. Genetics 151:331–341
Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32:W327–W331
Meeley RB, Briggs SP (1995) Reverse genetics for maize. Maize Genet Coop Newsl 69:67–82
Monforte AJ, Garcia-Mas J, Arús P (2003) Genetic variability in melon based on microsatellite variation. Plant Breeding 122:1–6
Mulder NJ, Apweiler R, Attwood TK, Bairoch A, Barrell D, Bateman A, Binns D, Biswas M, Bradley P, Bork P, et al. (2003) The InterPro Database, 2003 brings increased coverage and new features. Nucleic Acids Res 31:315–318
Murtas G, Reeves PH, Fu YF, Bancroft I, Dean C, Coupland G (2003) A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of small ubiquitin-related modifier conjugates. The Plant Cell 15:2308–2319
Ono A, Kim SH, Walbot V (2002) Subcellular localization of MURA and MURB proteins encoded by the maize MuDR transposon. Plant Mol Biol 50:599–611
Robertson DS (1978) Characterization of a Mutator system in maize. Mutat Res 51:21–28
Singer T, Yordan C, Martienssen RA (2001) Robertson’s Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev 15:591–602
Talbert LE, Chandler VL (1988) Characterization of a highly conserved sequence related to Mutator transposable elements in maize. Mol Biol Evol 5:519–529
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Turcotte K, Srinivasan S, Bureau T (2001) Survey of transposable elements from rice genomic sequences. Plant J 25:169–179
van Leeuwen H, Monfort A, Zhang HB, Puigdomènech P (2003) Identification and characterisation of a melon genomic region containing a resistance gene cluster from a constructed BAC library. Microcolinearity between Cucumis melo and Arabidopsis thaliana. Plant Mol Biol 51:703–718
van Leeuwen H, Garcia-Mas J, Coca M, Puigdoménech P, Monfort A (2005) Analysis of the melon genome in regions encompassing TIR-NBS-LRR resistance genes. Mol Genet Genomics 273:240–251
Xu Z, Yan X, Maurais S, Fu H, O’Brien DG, Mottinger J, Dooner HK (2004) Jittery, a Mutator distant relative with a paradoxical mobile behavior: excision without reinsertion. Plant Cell 16:1105–1114
Yu Z, Wright SI, Bureau TE (2000) Mutator-like elements in Arabidopsis thaliana. Structure, diversity and evolution. Genetics 156:2019–2031
Acknowledgments
The authors thank Mrs. Mercè Miquel for DNA sequencing and Dr. J.M. Casacuberta for helpful discussions. This project was funded by grant 2FD97-0286-(02-01) from CICYT and grant 2000FI-00316 to Hans van Leeuwen from CIRIT. This work was carried out within the framework of the Centre de Referència de Biotecnologia, Generalitat de Catalunya.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M.-A. Grandbastien.
Nucleotide sequence data reported are available in the GenBank database under the accession number AY524004.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
van Leeuwen, H., Monfort, A. & Puigdomenech, P. Mutator-like elements identified in melon, Arabidopsis and rice contain ULP1 protease domains. Mol Genet Genomics 277, 357–364 (2007). https://doi.org/10.1007/s00438-006-0194-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-006-0194-9