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Cloning and characterization of mariner-like elements in the soybean aphid, Aphis glycines Matsumura

Published online by Cambridge University Press:  12 May 2011

O. Mittapalli*
Affiliation:
Department of Entomology, The Ohio State University/Ohio Agricultural and Research Development Center, 1680 Madison Avenue, Wooster, OH 44691, USA
L. Rivera-Vega
Affiliation:
Department of Entomology, The Ohio State University/Ohio Agricultural and Research Development Center, 1680 Madison Avenue, Wooster, OH 44691, USA
B. Bhandary
Affiliation:
Department of Entomology, The Ohio State University/Ohio Agricultural and Research Development Center, 1680 Madison Avenue, Wooster, OH 44691, USA
M.A. Bautista
Affiliation:
Department of Entomology, The Ohio State University/Ohio Agricultural and Research Development Center, 1680 Madison Avenue, Wooster, OH 44691, USA
P. Mamidala
Affiliation:
Department of Entomology, The Ohio State University/Ohio Agricultural and Research Development Center, 1680 Madison Avenue, Wooster, OH 44691, USA
A.P. Michel
Affiliation:
Department of Entomology, The Ohio State University/Ohio Agricultural and Research Development Center, 1680 Madison Avenue, Wooster, OH 44691, USA
R.H. Shukle
Affiliation:
USDA-ARS and Department of Entomology, Purdue University, West Lafayette, IN 47907, USA
M.A.R. Mian
Affiliation:
USDA-ARS and Department of Horticulture and Crop Science, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA
*
*Authors for correspondence Fax: +01 330-263-3686 E-mail: [email protected]

Abstract

Soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is currently the most important insect pest of soybean (Glycine max (L.) Merr.) in the United States and causes significant economic damage worldwide, but little is known about the aphid at the molecular level. Mariner-like transposable elements (MLEs) are ubiquitous within the genomes of arthropods and various other invertebrates. In this study, we report the cloning of MLEs from the soybean aphid genome using degenerate PCR primers designed to amplify conserved regions of mariner transposases. Two of the ten sequenced clones (designated as Agmar1 and Agmar2) contained partial but continuous open reading frames, which shared high levels of homology at the protein level with other mariner transposases from insects and other taxa. Phylogenetic analysis revealed Agmar1 to group within the irritans subfamily of MLEs and Agmar2 within the mellifera subfamily. Southern blot analysis and quantitative PCR analysis indicated a low copy number for Agmar1-like elements within the soybean aphid genome. These results suggest the presence of at least two different putative mariner-like transposases encoded by the soybean aphid genome. Both Agmar1 and Agmar2 could play influential roles in the architecture of the soybean aphid genome. Transposable elements are also thought to potentially mediate resistance in insects through changes in gene amplification and mutations in coding sequences. Finally, Agmar1 and Agmar2 may represent useful genetic tools and provide insights on A. glycines adaptation.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2011

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References

Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403410.CrossRefGoogle ScholarPubMed
Augé-Gouillou, C., Notareschi-Leroy, H., Abad, P., Periquet, G. & Bigot, Y. (2000) Phylogenetic analysis of the functional domains of mariner-like element (MLE) transposases. Molecular and General Genetics 264, 506513.CrossRefGoogle Scholar
Barry, E.G., Witherspoon, D.J. & Lampe, D.J. (2004) A bacterial genetic screen identifies functional coding sequences of the insect mariner transposable element Famar 1 amplified from the genome of the earwig, Forficula auricularia. Genetics 166, 823833.CrossRefGoogle Scholar
Bryan, G.J., Jacobson, J.W. & Hartl, D.L. (1987) Heritable somatic excision of a Drosophila transposon. Science 235, 16361638.CrossRefGoogle ScholarPubMed
Bubner, B. & Baldwin, I.T. (2004) Use of real time PCR for determining copy number and zygosity in transgenic plants. Plant Cell Reports 23, 263271.Google Scholar
Capy, P., David, J.R. & Hartl, D.L. (1992) Evolution of the transposable element mariner in the Drososphila melanogaster species group. Genetica 86, 3746.CrossRefGoogle Scholar
Cooley, L., Kelley, R. & Sprading, A. (1988) Insertional mutagenesis of the Drosophila genome with single P elements. Science 239, 11211128.CrossRefGoogle ScholarPubMed
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 17921797.CrossRefGoogle ScholarPubMed
FAO Statistical Database (2010) FAOSTAT agriculture data. Available online at http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567#ancor (accessed 28 November 2010).Google Scholar
Feinberg, A.P. & Vogelstein, B. (1983) A technique for radiolabeing DNA restriction endonuclease fragments to high specific activity. Analytical Biochemistry 132, 613.CrossRefGoogle ScholarPubMed
Finston, T.L., Hebert, P.D.N. & Foottit, R. (1995) Genome size variation in aphids. Insect Biochemistry and Molecular Biology 25, 189196.Google Scholar
Hartl, D.L. (1989) Transposable element mariner in Drosophila species. pp. 531536 in Berg, D.E. & Howe, M.M. (Eds) Mobile DNA. Washington, DC, USA, American Society of Microbiology.Google Scholar
Hartl, D.L., Lohe, A.R. & Lozovskaya, E.R. (1997) Modern thoughts on an ancyent marinere: function, evolution, regulation. Annual Review of Genetics 31, 337358.Google Scholar
Hill, C.B., Li, Y. & Hartman, G.L. (2004) Resistance to the soybean aphid in soybean germplasm. Crop Science 44, 98106.Google Scholar
Hill, C.B., Crull, L., Herman, T.K., Voegtlin, D.J. & Hartman, G.L. (2010) A new soybean aphid (Hemiptera: Aphididae) biotype identified. Journal of Economic Entomology 103, 509515.Google Scholar
Izsvak, Z., Ivics, Z., Shimoda, N., Mohn, D., Okamoto, H. & Hackett, P.B. (1999) Short inverted-repeat transposable elements in teleost fish and implications for a mechanism of their amplification. Journal of Molecular Evolution 48, 1321.Google Scholar
Jacobson, J.W., Medhora, M.M. & Hartl, D.L. (1986) Molecular structure of a somatically unstable transposable element in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 83, 86848688.Google Scholar
Jarvik, T. & Lark, K.G. (1998) Characterization of Soymarl, a mariner element in soybean. Genetics 149, 15691574.CrossRefGoogle ScholarPubMed
Jurka, J., Kapitonov, V.V., Pavlicek, A., Klonowski, P., Kohany, O. & Walichiewicz, J. (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenetic and Genome Research 110, 462467.Google Scholar
Kim, K.S., Hill, C.B., Hartman, G.L., Mian, R.M. & Diers, B.W. (2008) Discovery of soybean aphid biotypes. Crop Science 48, 923928.Google Scholar
Lampe, D.J., Walden, K.K.O. & Robertson, H.M. (2001) Loss of transposase–DNA interaction may underlie the divergence of mariner family transposable elements and the ability of more than one mariner to occupy the same genome. Molecular Biology and Evolution 18, 954961.Google Scholar
Leroy, H., Leroy, F., Auge-Gouillou, C., Castagnone-Sereno, P. & Vanlerberghe-Masutti, F. (2000) Identification of mariner-like elements from the root-knot nematode Meloidogyne spp. Molecular and Biochemical Parasitology 107, 181190.Google Scholar
Li, X., Schuler, M.A. & Berenbaum, M.R. (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology 52, 231253.Google Scholar
Lidholm, D.A., Lohe, A.R. & Hartl, D.L. (1993) The transposable element mariner mediates germline transformation in Drosophila melanogaster. Genetics 134, 859868.CrossRefGoogle ScholarPubMed
Liu, D., Bischerour, J., Siddique, A., Buisine, N., Bigot, Y. & Chalmers, R. (2007) The human SETMAR protein preserves most of the activities of the ancestral Hsmar1 transposase. Molecular and Cellular Biology 27, 11251132.CrossRefGoogle ScholarPubMed
Maruyama, K. & Hartl, D.L. (1991) Evolution of the transposable element mariner in Drosophila species. Genetics 128, 319329.Google Scholar
Medhora, M., Maruyana, K. & Hartl, D.L. (1991) Molecular and functional analysis of the mariner mutator element Mos1 in Drosophila. Genetics 128, 311318.Google Scholar
Mensah, C., DiFonzo, C., Nelson, R.L. & Wang, D. (2005) Resistance to soybean aphid in early maturing soybean germplasm. Crop Science 45, 22282233.Google Scholar
Mian, M.A.R., Hammond, R.B. & Martin, S.K. (2008a) New plant introductions with resistance to the soybean aphid. Crop Science 48, 10551061.Google Scholar
Mian, M.A.R., Kang, S.-T., Beil, S.E. & Hammond, R.B. (2008b) Genetic linkage mapping of the soybean aphid resistance gene in PI 243540. Theoretical and Applied Genetics 117, 955962.Google Scholar
Mittapalli, O., Shukle, R.H. & Wise, I.L. (2006) Identification of mariner-like elements in Sitodiplosis mosellana (Diptera: Cecidomyiidae). Canadian Entomologist 138, 138146.Google Scholar
Moran, N.A., Degnan, P.H., Santos, S.R., Dunbar, H.E. & Ochman, H. (2005) The players in a mutualistic symbiosis: Insects, bacteria, viruses and virulence genes. Proceedings of the National Academy of Sciences 102, 1691916926.CrossRefGoogle Scholar
Muñoz-Lopez, M., Siddique, A., Bischerour, J., Lorite, P., Chalmers, R. & Palomeque, T. (2008) Transposition of Mboumar-9: identification of a new naturally active mariner-family transposon. Journal of Molecular Biology 382, 567572.Google Scholar
Nikoh, N., McCutcheon, J.P., Kudo, T., Miyagishima, S., Moran, N.A. & Nakabochi, A. (2010) Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its hosts. PLoS Genetics 6, e1000827.CrossRefGoogle Scholar
Ragsdale, D.W., McCornack, B.P., Venette, R.C., Potter, B.D., MacRae, I.V., Hodgson, E.W., O'Neal, M.E., Johnson, K.D., O'Neil, R.J., DiFonzo, C.D., Hunt, T.E., Glogoza, P.A. & Cullen, E.M. (2007) Economic threshold for soybean aphid (Hemiptera: Aphididae). Journal of Economic Entomology 100, 12581267.Google Scholar
Robertson, H.M. (1993) The mariner transposable element is widespread in insects. Nature 362, 241245.Google Scholar
Robertson, H.M. & Lampe, D.J. (1995a) Distribution of transposable elements in arthropods. Annual Review of Entomology 40, 333357.CrossRefGoogle ScholarPubMed
Robertson, H.M. & Lampe, D.J. (1995b) Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera. Molecular Biology and Evolution 12, 850862.Google ScholarPubMed
Robertson, H.M. & MacLeod, E.G. (1993) Five major subfamilies of mariner transposable elements in insects, including the Mediterranean fruit fly, and related arthropods. Insect Molecular Biology 2, 125139.Google Scholar
Sambrook, J. & Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. 3rd edn. Cold Spring Harbor, NY, USA, Cold Spring Harbor Laboratory Press.Google Scholar
Schneider, D., Faure, D., Noirclerc-Savoye, M., Barriere, A.C., Coursange, E. & Blot, M. (2000) A broad-host-range plasmid for isolating mobile genetic elements in gram-negative bacteria. Plasmid 44, 201207.Google Scholar
Shukle, R.H. & Russell, V.W. (1995) Mariner transposase-like sequences from the Hessian fly, Mayetiola destructor. Journal of Heredity 86, 364368.CrossRefGoogle ScholarPubMed
Simmons, G.M. (1992) Horizontal transfer of hobo transposable elements within the Drosophila melanogaster species complex, evidence from DNA sequencing. Molecular Biology and Evolution 9, 10501060.Google Scholar
Solomon, P.S., Ipcho, S.V.S., Hane, J.K., Tan, K.C. & Oliver, R.P. (2008) A quantitative PCR approach to determine gene copy number. Fungal Genetics Reports 55, 58.CrossRefGoogle Scholar
Strausbaugh, L.D., Bourke, M.T., Sommer, M.T., Coon, M.E. & Berg, C.M. (1990) Probe mapping to facilitate transposon-based DNA sequencing. Proceedings of the National Academy of Sciences of the United States of America 87, 62136217.Google Scholar
Swofford, D.L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4. Sunderland, MA, USA, Sinauer Associates.Google Scholar
TIAGC (The International Aphid Genomics Consortium) (2010) Genome Sequence of the Pea Aphid Acyrthosiphon pisum. PLoS Biology 8, e1000313.Google Scholar
Thompson, J.D., Gibson, T.J., Plewniak, F. & Jeanmougin, F. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.Google Scholar
Venette, R.C. & Ragsdale, D.W. (2004) Assessing the invasion by soybean aphid (Homoptera: Aphididae): Where will it end? Annals of the Entomological Society of America 97, 219226.CrossRefGoogle Scholar
Wu, Z., Schenk-Hamlin, D., Zhan, W., Ragsdale, D.W. & Heimpel, G.E. (2004) The soybean aphid in China: an historical review. Annals of the Entomological Society of America 97, 209218.CrossRefGoogle Scholar
Zhang, G.R., Gu, C.H. & Wang, D.C. (2009) Molecular mapping of soybean aphid resistance genes in PI 567541B. Theoretical and Applied Genetics 118, 473482.Google Scholar