Replication of Nonautonomous Retroelements in Soybean Appears to Be Both Recent and Common

Retrotransposons and their remnants often constitute more than 50% of higher plant genomes. Although extensively studied in monocot crops such as maize (Zea mays) and rice (Oryza sativa), the impact of retrotransposons on dicot crop genomes is not well documented. Here, we present an analysis of ret...

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Published in	Plant physiology (Bethesda) Vol. 148; no. 4; pp. 1760 - 1771
Main Authors	Wawrzynski, Adam, Ashfield, Tom, Chen, Nicolas W.G, Mammadov, Jafar, Nguyen, Ashley, Podicheti, Ram, Cannon, Steven B, Thareau, Vincent, Ameline-Torregrosa, Carine, Cannon, Ethalinda, Chacko, Ben, Couloux, Arnaud, Dalwani, Anita, Denny, Roxanne, Deshpande, Shweta, Egan, Ashley N, Glover, Natasha, Howell, Stacy, Ilut, Dan, Lai, Hongshing, del Campo, Sara Martin, Metcalf, Michelle, O'Bleness, Majesta, Pfeil, Bernard E, Ratnaparkhe, Milind B, Samain, Sylvie, Sanders, Iryna, Ségurens, Béatrice, Sévignac, Mireille, Sherman-Broyles, Sue, Tucker, Dominic M, Yi, Jing, Doyle, Jeff J, Geffroy, Valérie, Roe, Bruce A, Maroof, M.A. Saghai, Young, Nevin D, Innes, Roger W
Format	Journal Article
Language	English
Published	Rockville, MD American Society of Plant Biologists 01.12.2008
Subjects	Base Sequence beans Biological and medical sciences chemistry Corn crops DNA, Plant DNA, Plant - chemistry Evolution Evolution, Molecular Fundamental and applied biological sciences. Psychology Gene Deletion genetics Genome Analysis Genome, Plant Genomes Genomics Genomics - methods Glycine max Glycine max - genetics Glycine tomentella homologous recombination Long Interspersed Nucleotide Elements methods Methylation Mutagenesis, Insertional mutation Neonotonia wightii Oryza sativa Phaseolus Phaseolus - genetics Phaseolus vulgaris Phylogeny Plant physiology and development planting date Plants Retroelements Retrotransposons Rice Sequence Alignment Sequence Analysis, DNA Soybeans Terminal Repeat Sequences Transposons wild relatives Zea mays Grain legume Leguminosae Plant physiology Dicotyledones Angiospermae Replication Spermatophyta Soybean Glycine max
Online Access	Get full text
ISSN	0032-0889 1532-2548 1532-2548
DOI	10.1104/pp.108.127910

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Abstract	Retrotransposons and their remnants often constitute more than 50% of higher plant genomes. Although extensively studied in monocot crops such as maize (Zea mays) and rice (Oryza sativa), the impact of retrotransposons on dicot crop genomes is not well documented. Here, we present an analysis of retrotransposons in soybean (Glycine max). Analysis of approximately 3.7 megabases (Mb) of genomic sequence, including 0.87 Mb of pericentromeric sequence, uncovered 45 intact long terminal repeat (LTR)-retrotransposons. The ratio of intact elements to solo LTRs was 8:1, one of the highest reported to date in plants, suggesting that removal of retrotransposons by homologous recombination between LTRs is occurring more slowly in soybean than in previously characterized plant species. Analysis of paired LTR sequences uncovered a low frequency of deletions relative to base substitutions, indicating that removal of retrotransposon sequences by illegitimate recombination is also operating more slowly. Significantly, we identified three subfamilies of nonautonomous elements that have replicated in the recent past, suggesting that retrotransposition can be catalyzed in trans by autonomous elements elsewhere in the genome. Analysis of 1.6 Mb of sequence from Glycine tomentella, a wild perennial relative of soybean, uncovered 23 intact retroelements, two of which had accumulated no mutations in their LTRs, indicating very recent insertion. A similar pattern was found in 0.94 Mb of sequence from Phaseolus vulgaris (common bean). Thus, autonomous and nonautonomous retrotransposons appear to be both abundant and active in Glycine and PHASEOLUS: The impact of nonautonomous retrotransposon replication on genome size appears to be much greater than previously appreciated.
AbstractList	Retrotransposons and their remnants often constitute more than 50% of higher plant genomes. Although extensively studied in monocot crops such as maize (Zea mays) and rice (Oryza sativa), the impact of retrotransposons on dicot crop genomes is not well documented. Here, we present an analysis of retrotransposons in soybean (Glycine max). Analysis of approximately 3.7 megabases (Mb) of genomic sequence, including 0.87 Mb of pericentromeric sequence, uncovered 45 intact long terminal repeat (LTR)-retrotransposons. The ratio of intact elements to solo LTRs was 8:1, one of the highest reported to date in plants, suggesting that removal of retrotransposons by homologous recombination between LTRs is occurring more slowly in soybean than in previously characterized plant species. Analysis of paired LTR sequences uncovered a low frequency of deletions relative to base substitutions, indicating that removal of retrotransposon sequences by illegitimate recombination is also operating more slowly. Significantly, we identified three subfamilies of nonautonomous elements that have replicated in the recent past, suggesting that retrotransposition can be catalyzed in trans by autonomous elements elsewhere in the genome. Analysis of 1.6 Mb of sequence from Glycine tomentella, a wild perennial relative of soybean, uncovered 23 intact retroelements, two of which had accumulated no mutations in their LTRs, indicating very recent insertion. A similar pattern was found in 0.94 Mb of sequence from Phaseolus vulgaris (common bean). Thus, autonomous and nonautonomous retrotransposons appear to be both abundant and active in Glycine and PHASEOLUS: The impact of nonautonomous retrotransposon replication on genome size appears to be much greater than previously appreciated. Retrotransposons and their remnants often constitute more than 50% of higher plant genomes. Although extensively studied in monocot crops such as maize ( Zea mays ) and rice ( Oryza sativa ), the impact of retrotransposons on dicot crop genomes is not well documented. Here, we present an analysis of retrotransposons in soybean ( Glycine max ). Analysis of approximately 3.7 megabases (Mb) of genomic sequence, including 0.87 Mb of pericentromeric sequence, uncovered 45 intact long terminal repeat (LTR)-retrotransposons. The ratio of intact elements to solo LTRs was 8:1, one of the highest reported to date in plants, suggesting that removal of retrotransposons by homologous recombination between LTRs is occurring more slowly in soybean than in previously characterized plant species. Analysis of paired LTR sequences uncovered a low frequency of deletions relative to base substitutions, indicating that removal of retrotransposon sequences by illegitimate recombination is also operating more slowly. Significantly, we identified three subfamilies of nonautonomous elements that have replicated in the recent past, suggesting that retrotransposition can be catalyzed in trans by autonomous elements elsewhere in the genome. Analysis of 1.6 Mb of sequence from Glycine tomentella , a wild perennial relative of soybean, uncovered 23 intact retroelements, two of which had accumulated no mutations in their LTRs, indicating very recent insertion. A similar pattern was found in 0.94 Mb of sequence from Phaseolus vulgaris (common bean). Thus, autonomous and nonautonomous retrotransposons appear to be both abundant and active in Glycine and Phaseolus . The impact of nonautonomous retrotransposon replication on genome size appears to be much greater than previously appreciated. Retrotransposons and their remnants often constitute more than 50% of higher plant genomes. Although extensively studied in monocot crops such as maize (Zea mays) and rice (Oryza sativa), the impact of retrotransposons on dicot crop genomes is not well documented. Here, we present an analysis of retrotransposons in soybean (Glycine max). Analysis of approximately 3.7 megabases (Mb) of genomic sequence, including 0.87 Mb of pericentromeric sequence, uncovered 45 intact long terminal repeat (LTR)-retrotransposons. The ratio of intact elements to solo LTRs was 8:1, one of the highest reported to date in plants, suggesting that removal of retrotransposons by homologous recombination between LTRs is occurring more slowly in soybean than in previously characterized plant species. Analysis of paired LTR sequences uncovered a low frequency of deletions relative to base substitutions, indicating that removal of retrotransposon sequences by illegitimate recombination is also operating more slowly. Significantly, we identified three subfamilies of nonautonomous elements that have replicated in the recent past, suggesting that retrotransposition can be catalyzed in trans by autonomous elements elsewhere in the genome. Analysis of 1.6 Mb of sequence from Glycine tomentella, a wild perennial relative of soybean, uncovered 23 intact retroelements, two of which had accumulated no mutations in their LTRs, indicating very recent insertion. A similar pattern was found in 0.94 Mb of sequence from Phaseolus vulgaris (common bean). Thus, autonomous and nonautonomous retrotransposons appear to be both abundant and active in Glycine and Phaseolus. The impact of nonautonomous retrotransposon replication on genome size appears to be much greater than previously appreciated.Retrotransposons and their remnants often constitute more than 50% of higher plant genomes. Although extensively studied in monocot crops such as maize (Zea mays) and rice (Oryza sativa), the impact of retrotransposons on dicot crop genomes is not well documented. Here, we present an analysis of retrotransposons in soybean (Glycine max). Analysis of approximately 3.7 megabases (Mb) of genomic sequence, including 0.87 Mb of pericentromeric sequence, uncovered 45 intact long terminal repeat (LTR)-retrotransposons. The ratio of intact elements to solo LTRs was 8:1, one of the highest reported to date in plants, suggesting that removal of retrotransposons by homologous recombination between LTRs is occurring more slowly in soybean than in previously characterized plant species. Analysis of paired LTR sequences uncovered a low frequency of deletions relative to base substitutions, indicating that removal of retrotransposon sequences by illegitimate recombination is also operating more slowly. Significantly, we identified three subfamilies of nonautonomous elements that have replicated in the recent past, suggesting that retrotransposition can be catalyzed in trans by autonomous elements elsewhere in the genome. Analysis of 1.6 Mb of sequence from Glycine tomentella, a wild perennial relative of soybean, uncovered 23 intact retroelements, two of which had accumulated no mutations in their LTRs, indicating very recent insertion. A similar pattern was found in 0.94 Mb of sequence from Phaseolus vulgaris (common bean). Thus, autonomous and nonautonomous retrotransposons appear to be both abundant and active in Glycine and Phaseolus. The impact of nonautonomous retrotransposon replication on genome size appears to be much greater than previously appreciated.
Author	Nguyen, Ashley Innes, Roger W Ségurens, Béatrice Doyle, Jeff J Lai, Hongshing Geffroy, Valérie Cannon, Ethalinda Glover, Natasha Yi, Jing Couloux, Arnaud Howell, Stacy Roe, Bruce A Young, Nevin D Dalwani, Anita Samain, Sylvie Chacko, Ben Thareau, Vincent O'Bleness, Majesta del Campo, Sara Martin Pfeil, Bernard E Chen, Nicolas W.G Tucker, Dominic M Maroof, M.A. Saghai Egan, Ashley N Ratnaparkhe, Milind B Podicheti, Ram Cannon, Steven B Wawrzynski, Adam Ilut, Dan Metcalf, Michelle Ameline-Torregrosa, Carine Denny, Roxanne Deshpande, Shweta Sanders, Iryna Sévignac, Mireille Ashfield, Tom Sherman-Broyles, Sue Mammadov, Jafar
AuthorAffiliation	Department of Biology, Indiana University, Bloomington, Indiana 47405 (A.W., T.A., R.P., A.D., S.H., S.M.d.C., M.M., R.W.I.); Institut de Biotechnologie des Plantes, UMR CNRS 8618, INRA, Université Paris Sud, 91 405 Orsay, France (N.W.G.C., V.T., M.S., V.G.); Department of Crop and Soil Environmental Sciences, Virginia Tech, Blacksburg, Virginia 24061 (J.M., A.N., N.G., M.B.R., D.M.T., M.A.S.M.); Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota 55108 (S.B.C., C.A.-T., E.C., B.C., R.D., N.D.Y.); U.S. Department of Agriculture-Agricultural Research Service and Department of Agronomy (S.B.C.), and Virtual Reality Application Center (E.C.), Iowa State University, Ames, Iowa 50011; Genoscope/CEA-Centre National de Séquençage, 91 057 Evry, France (A.C., S.S., B.S.); Department of Chemistry and Biochemistry, University of Oklahoma, Norman, Oklahoma 73019 (S.D., H.L., M.O., I.S., J.Y., B.A.R.); L.H. Bailey Hortorium, Department of Plant Biology, Cornell University, I
AuthorAffiliation_xml	– name: Department of Biology, Indiana University, Bloomington, Indiana 47405 (A.W., T.A., R.P., A.D., S.H., S.M.d.C., M.M., R.W.I.); Institut de Biotechnologie des Plantes, UMR CNRS 8618, INRA, Université Paris Sud, 91 405 Orsay, France (N.W.G.C., V.T., M.S., V.G.); Department of Crop and Soil Environmental Sciences, Virginia Tech, Blacksburg, Virginia 24061 (J.M., A.N., N.G., M.B.R., D.M.T., M.A.S.M.); Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota 55108 (S.B.C., C.A.-T., E.C., B.C., R.D., N.D.Y.); U.S. Department of Agriculture-Agricultural Research Service and Department of Agronomy (S.B.C.), and Virtual Reality Application Center (E.C.), Iowa State University, Ames, Iowa 50011; Genoscope/CEA-Centre National de Séquençage, 91 057 Evry, France (A.C., S.S., B.S.); Department of Chemistry and Biochemistry, University of Oklahoma, Norman, Oklahoma 73019 (S.D., H.L., M.O., I.S., J.Y., B.A.R.); L.H. Bailey Hortorium, Department of Plant Biology, Cornell University, Ithaca, New York 14853 (A.N.E., D.I., B.E.P., S.S.-B., J.J.D.); CSIRO Plant Industry, Canberra, Australian Capital Territory 2601, Australia (B.E.P.); and Division of Plant Sciences, University of Missouri, Columbia, Missouri 65211 (M.B.R.)
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Keywords	Grain legume Leguminosae Plant physiology Dicotyledones Angiospermae Replication Spermatophyta Soybean Glycine max
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Open access articles can be viewed online without a subscription. The online version of this article contains Web-only data. This work was supported by the National Science Foundation (Plant Genome Research Program grant no. DBI–0321664 to R.W.I., M.A.S.M., N.D.Y., B.A.R., and J.J.D. and Systematics award no. DEB–0516673 to A.N.E.) and by Genoscope/CEA-Centre National de Séquençage (grant to V.G.). www.plantphysiol.org/cgi/doi/10.1104/pp.108.127910 The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Roger W. Innes (rinnes@indiana.edu). Present address: Trait Genetics and Technology, Dow AgroSciences LLC, Indianapolis, IN 46268. Corresponding author; e-mail rinnes@indiana.edu.
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Snippet	Retrotransposons and their remnants often constitute more than 50% of higher plant genomes. Although extensively studied in monocot crops such as maize (Zea... Retrotransposons and their remnants often constitute more than 50% of higher plant genomes. Although extensively studied in monocot crops such as maize ( Zea...
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SubjectTerms	Base Sequence beans Biological and medical sciences chemistry Corn crops DNA, Plant DNA, Plant - chemistry Evolution Evolution, Molecular Fundamental and applied biological sciences. Psychology Gene Deletion genetics Genome Analysis Genome, Plant Genomes Genomics Genomics - methods Glycine max Glycine max - genetics Glycine tomentella homologous recombination Long Interspersed Nucleotide Elements methods Methylation Mutagenesis, Insertional mutation Neonotonia wightii Oryza sativa Phaseolus Phaseolus - genetics Phaseolus vulgaris Phylogeny Plant physiology and development planting date Plants Retroelements Retrotransposons Rice Sequence Alignment Sequence Analysis, DNA Soybeans Terminal Repeat Sequences Transposons wild relatives Zea mays
Title	Replication of Nonautonomous Retroelements in Soybean Appears to Be Both Recent and Common
URI	https://www.jstor.org/stable/40066307 https://www.ncbi.nlm.nih.gov/pubmed/18952860 https://www.proquest.com/docview/48162884 https://www.proquest.com/docview/69871885 https://pubmed.ncbi.nlm.nih.gov/PMC2593652
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