Abstract
The maize Ac/Ds transposable element (TE) transposes by a “cut and paste” mechanism. Previous studies in maize showed that when the TE ends are in reversed orientation with respect to each other, alternative transposition reactions can occur resulting in large scale genome rearrangements including deletions and inversions. To test whether similar genome rearrangements can also occur in other plants, we studied the efficacy of such alternative transposition-mediated genome rearrangements in Arabidopsis. Here we present our analysis of 33 independent chromosome rearrangements. Transposition at the reversed ends Ds element can cause deletions over 1 Mbp, and inversions up to 2.4 Mbp in size. We identified additional rearrangements including a reciprocal translocation and a putative ring chromosome. Some of the deletions and inversions are germinally transmitted.
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References
Bancroft I, Dean C (1993) Factors affecting the excision frequency of maize transposable element Ds in Arabidopsis thaliana. Mol Gen Genet 240:65–72. doi:10.1007/BF00276885
Bayley CC, Morgan M, Dale EC, Ow DW (1992) Exchange of gene activity in transgenic plants catalyzed by the Cre-lox site-specific recombination system. Plant Mol Biol 18(2):353–361. doi:10.1007/BF00034962
Britton MT, Escobar MA, Dandekar AM (2008) The oncogenes of Agrobacterium Tumefaciens and Agrobacterium Rhizogenes. In: Tzfira T, Citovsky V (eds) Agrobacterium: from biology to biotechnology, Springer, New York, pp 523–563
Burr B, Burr FA (1982) Ds controlling elements of maize at the shrunken locus are large and dissimilar insertions. Cell 29(3):977–986. doi:10.1016/0092-8674(82)90461-5
Carroll BJ, Klimyuk VI, Thomas CM, Bishop GJ, Harrison K, Scofield SR et al (1995) Germinal transpositions of the maize element dissociation from T-DNA loci in tomato. Genetics 139:407–420
Chaleff D, Mauvais J, McCormick S, Shure M, Wessler S, Fedoroff N (1981) Controlling elements in maize. Carnegie Inst Wash Yearb 80:158–174
Chen J, Greenblatt IM, Dellaporta SL (1987) Transposition of Ac from the P locus of maize into unreplicated chromosomal sites. Genetics 117(1):109–116
Chen J, Greenblatt IM, Dellaporta SL (1992) Molecular analysis of Ac transposition and DNA replication. Genetics 130(3):665–676
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743. doi:10.1046/j.1365-313x.1998.00343.x
Coupland G, Plum C, Chatterjee S, Post A, Starlinger P (1989) Sequences near the termini are required for transposition of the maize transposon Ac in transgenic tobacco plants. Proc Natl Acad Sci USA 86(23):9385–9388. doi:10.1073/pnas.86.23.9385
Courage-Tebbe U, Doring HP, Fedoroff N, Starlinger P (1983) The controlling element Ds at the Shrunken locus in Zea mays: structure of the unstable sh-m5933 allele and several revertants. Cell 34(2):383–393. doi:10.1016/0092-8674(83)90372-0
Dale EC, Ow DW (1990) Intra- and intermolecular site-specific recombination in plant cells mediated by bacteriophage P1 recombinase. Gene 91(1):79–85. doi:10.1016/0378-1119(90)90165-N
Doring HP, Nelsen-Salz B, Garber R, Tillman E (1981) Double Ds elements are involved in specific chromosome breakage. Mol Gen Genet 219(1–2):299–305
English J, Harrison K, Jones JD (1993) A genetic analysis of DNA sequence requirements for dissociation state I activity in tobacco. Plant Cell 5:501–514
English JJ, Harrison K, Jones J (1995) Aberrant transpositions of maize double Ds-like elements usually involve Ds ends on sister chromatids. Plant Cell 7(8):1235–1247
Gorbunova V, Levy AA (1997) Circularized Ac/Ds transposons: formation, structure and fate. Genetics 145:1161–1169
Greenblatt IM (1984) A chromosome replication pattern deduced from pericarp phenotypes resulting from movements of the transposable element, modulator, in maize. Genetics 108(2):471–485
Greenblatt IM, Brink RA (1962) Twin mutations in medium variegated pericarp maize. Genetics 47(4):489–501
Hehl R, Baker B (1990) Properties of the maize transposable element Activator in transgenic tobacco plants: a versatile inter-species genetic tool. Plant Cell 2(8):709–721
Hentges KE, Justice MJ (2004) Checks and balancers: balancer chromosomes to facilitate genome annotation. Trends Genet 20(6):252–259. doi:10.1016/j.tig.2004.04.004
Honma MA, Baker BJ, Waddell CS (1993) High-frequency germinal transposition of Ds ALS in Arabidopsis. Proc Natl Acad Sci USA 90(13):6242–6246. doi:10.1073/pnas.90.13.6242
Ito T, Motohashi R, Kuromori T, Noutoshi Y, Seki M, Kamiya A et al (2005) A resource of 5,814 dissociation transposon-tagged and sequence-indexed lines of Arabidopsis transposed from start loci on chromosome 5. Plant Cell Physiol 46(7):1149–1153. doi:10.1093/pcp/pci112
Jones RN (2005) McClintock’s controlling elements: the full story. Cytogenet Genome Res 109(1–3):90–103. doi:10.1159/000082387
Kunze R, Weil CF (2002) The hAT and CACTA superfamilies of plant transposons. In: Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) Mobile DNA II. ASM Press, Washington, DC, pp 565–610
Kuromori T, Hirayama T, Kiyosue Y, Takabe H, Mizukado S, Sakurai T et al (2004) A collection of 11 800 single-copy Ds transposon insertion lines in Arabidopsis. Plant J 37(6):897–905. doi:10.1111/j.1365.313X.2004.02009.x
Laufs P, Autran D, Traas J (1999) A chromosomal paracentric inversion associated with T-DNA integration in Arabidopsis. Plant J 18(2):131–139. doi:10.1046/j.1365-313X.1999.00436.x
Li ZW, Stark G, Gotz J, Rulicke T, Gschwind M, Huber G et al (1996) Generation of mice with a 200-kb amyloid precursor protein gene deletion by Cre recombinase-mediated site-specific recombination in embryonic stem cells. Proc Natl Acad Sci USA 93(12):6158–6162. doi:10.1073/pnas.93.12.6158
Martinez-Ferez IM, Dooner HK (1997) Sesqui-Ds, the chromosome-breaking insertion at bz-m1, links double Ds to the original Ds element. Mol Gen Genet 255(6):580–586. doi:10.1007/s004380050531
Medberry SL, Dale E, Qin M, Ow DW (1995) Intra-chromosomal rearrangements generated by Cre-lox site-specific recombination. Nucleic Acids Res 23(3):485–490. doi:10.1093/nar/23.3.485
Muller HJ (1918) Genetic variability, twin hybrids and constant hybrids, in a case of balanced lethal factors. Genetics 3:422–499
Müller-Neumann M, Yoder JI, Starlinger P (1984) The DNA sequence of the transposable element Ac of Zea mays L. Mol Gen Genet 198:19–24. doi:10.1007/BF00328695
Nacry P, Camilleri C, Courtial B, Caboche M, Bouchez D (1998) Major chromosomal rearrangements induced by T-DNA transformation in Arabidopsis. Genetics 149(2):641–650
Osborne BI, Wirtz U, Baker B (1995) A system for insertional mutagenesis and chromosomal rearrangement using the Ds transposon and Cre-lox. Plant J 7(4):687–701. doi:10.1046/j.1365-313X.1995.7040687.x
Page DR, Kohler C, Da Costa-Nunes JA, Baroux C, Moore JM, Grossniklaus U (2004) Intrachromosomal excision of a hybrid Ds element induces large genomic deletions in Arabidopsis. Proc Natl Acad Sci U S A. 101:2969–2974
Panjabi P, Burma PK, Pental D (2006) Use of the transposable element Ac/Ds in conjunction with Spm/dSpm for gene tagging allows extensive genome coverage with a limited number of starter lines: functional analysis of a four-element system in Arabidopsis thaliana. Mol Gen Genomics 276(6): 533–543
Pohlman RF, Fedoroff NV, Messing J (1984) The nucleotide sequence of the maize controlling element Activator. Cell 37(2):635–643. doi:10.1016/0092-8674(84)90395-7
Ralston E, English J, Dooner HK (1989) Chromosome-breaking structure in maize involving a fractured Ac element. Proc Natl Acad Sci USA 86(23):9451–9455. doi:10.1073/pnas.86.23.9451
Ramirez-Solis R, Liu P, Bradley A (1995) Chromosome engineering in mice. Nature 378(6558):720–724. doi:10.1038/378720a0
Russell SH, Hoopes JL, Odell JT (1992) Directed excision of a transgene from the plant genome. Mol Gen Genet 234(1):49–59
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
Swinburne J, Balcells L, Scofield SR, Jones JD, Coupland G (1992) Elevated levels of Activator transposase mRNA are associated with high frequencies of Dissociation excision in Arabidopsis. Plant Cell 4(5):583–595
Tax FE, Vernon DM (2001) T-DNA-associated duplication/translocations in Arabidopsis. Implications for mutant analysis and functional genomics. Plant Physiol 126(4):1527–1538. doi:10.1104/pp.126.4.1527
Wagner KU, Wall RJ, St-Onge L, Gruss P, Wynshaw-Boris A, Garrett L et al (1997) Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res 25(21):4323–4330. doi:10.1093/nar/25.21.4323
Wang L, Heinlein M, Kunze R (1996) Methylation pattern of Activator transposase binding sites in maize endosperm. Plant Cell 8(4):747–758
Weck E, Courage U, Doring HP, Fedoroff N, Starlinger P (1984) Analysis of sh-m6233, a mutation induced by the transposable element Ds in the sucrose synthase gene of Zea mays. EMBO J 3(8):1713–1716
Weil CF, Wessler SR (1993) Molecular evidence that chromosome breakage by Ds elements is caused by aberrant transposition. Plant Cell 5(5):515–522. doi:10.1105/tpc.5.5.515
Woody ST, Austin-Phillips S, Amasino RM, Krysan PJ (2007) The WiscDsLox T-DNA collection: an arabidopsis community resource generated by using an improved high-throughput T-DNA sequencing pipeline. J Plant Res 120(1):157–165. doi:10.1007/s10265-006-0048-x
Xiang C, Han P, Lutziger I, Wang K, Oliver DJ (1999) A mini binary vector series for plant transformation. Plant Mol Biol 40(4):711–717. doi:10.1023/A:1006201910593
Zeh K, Andahazy M, O’Gorman S, Baribault H (1998) Selection of primary cell cultures with cre recombinase induced somatic mutations from transgenic mice. Nucleic Acids Res 26(18):4301–4303. doi:10.1093/nar/26.18.4301
Zhang J, Peterson T (1999) Genome rearrangements by nonlinear transposons in maize. Genetics 153(3):1403–1410
Zhang J, Peterson T (2004) Transposition of reversed Ac element ends generates chromosome rearrangements in maize. Genetics 167(4):1929–1937. doi:10.1534/genetics.103.026229
Zhang J, Peterson T (2005) A segmental deletion series generated by sister-chromatid transposition of Ac transposable elements in maize. Genetics 171(1):333–344. doi:10.1534/genetics.104.035576
Zhang S, Raina S, Li H, Li J, Dec E, Ma H et al (2003) Resources for targeted insertional and deletional mutagenesis in Arabidopsis. Plant Mol Biol 53(1–2):133–150. doi:10.1023/B:PLAN.0000009271.08420.d9
Acknowledgements
We thank R. Martienssen for plasmid pAJ6, D. Voytas and D. Wright for plasmid pDW418, and C. Waddell for Arabidopsis plants carrying rbcS:Ac-1017. Lisa Coffey, Tanya Rogers, Peter Howe, Avni Sanghi and Michelle Blessington assisted with various aspects of this study. This research was supported by NSF Award 0110170 to T.P.
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Krishnaswamy, L., Zhang, J. & Peterson, T. Reversed end Ds element: a novel tool for chromosome engineering in Arabidopsis. Plant Mol Biol 68, 399–411 (2008). https://doi.org/10.1007/s11103-008-9377-6
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DOI: https://doi.org/10.1007/s11103-008-9377-6