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

Authors: WAWRZYNSKI, ADAM - INDIANA UNIV; ASHFIELD, TOM - INDIANA UNIV; CHEN, NICOLAS - CNRS, ORSAY, FRANCE; MAMMADOV, JAFAR - VIRGINIA TECH; NGUYEN, ASHLEY - VIRGINIA TECH; PODICHETI, RAM - INDIANA UNIV; Cannon, Steven; THAREAU, VINCENT - CNRS, ORSAY, FRANCE; AMELINE-TORREGROSA, CARINE - UNIV MINNESOTA; CANNON, ETHALINDA - ISU; CHACKO, BEN - UNIV MINNESOTA; COULOUX, ARNAUD - CNS, EVRY, FRANCE; DALWANI, ANITA - INDIANA UNIV; DENNY, ROXANNE - UNIV MINNESOTA; DESHPANDE, SHWETA - UNIV OKLAHOMA; EGAN, ASHLEY - CORNELL UNIV; GLOVER, NATASHA - VIRGINIA TECH; HOWELL, STACY - INDIANA UNIV; ILUT, DAN - CORNELL UNIV; LAI, HOHNSHING - UNIV OKLAHOMA; MARTIN DEL CAMPO, SARA - INDIANA UNIV; METCALF, MICHELLE - INDIANA UNIV; O'BLENESS, MAJESTA - UNIV OKLAHOMA; PFEIL, BERNARD - CSIRO; RATNAPARKHE, MILIND - UNIV MISSOURI; ROE, BRUCE - UNIV OKLAHOMA; MAROOF, M.A. SAGHAI - VIRGINIA TECH; SAMAIN, SYLVIE - CNS, EVRY, FRANCE; SANDERS, IRYNA - UNIV OKLAHOMA; SEGURENS, BEATRICE - CNS, EVRY, FRANCE; SEVIGNAC, MIREILLE - CNS, EVRY, FRANCE; SHERMAN-BROYLES, SUE - CORNELL UNIV; TUCKER, DOMINIC - VIRGINIA TECH; YI, JING - CNS, EVRY, FRANCE; DOYLE, JEFF - CORNELL UNIV; GEFFROY, VALERIE - INRA, ORSAY, FRANCE; ROE, BRUCE - UNIV OKLAHOMA; MAROOF, M.A. SGHAI - VIRGINIA TECH; YOUNG, NEVIN - UNIV MINNESOTA; INNES, ROGER - INDIANA UNIV

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/22/2008
Publication Date: 10/24/2008
Citation: Wawrzynski, A., Ashfield, T., Chen, N.W., Mammadov, J., Nguyen, A., Podicheti, R., Cannon, S.B., Thareau, V., Ameline-Torregrosa, C., Cannon, E., Chacko, B., Couloux, A., Dalwani, A., Denny, R., Deshpande, S., Egan, A., Glover, N., Howell, S., Ilut, D., Lai, H., Martin Del Campo, S., Metcalf, M., O'Bleness, M., Pfeil, B., Ratnaparkhe, M., Roe, B., Maroof, M., Samain, S., Sanders, I., Segurens, B., Sevignac, M., Sherman-Broyles, S., Tucker, D.M., Yi, J., Doyle, J.J., Geffroy, V., Roe, B., Maroof, M., Young, N., Innes, R.W. 2008. Replication of Nonautonomous Retroelements in Soybean Appears to be Both Recent and Common. Plant Physiology. 148:1760-1771.

Interpretive Summary: A plant's genome, comprised of all the DNA in a cell, contains the genetic blueprint required to produce the plant itself. A decades-old puzzle for biologists is that the majority of this DNA sequence in any higher organism consists not of genes (which encode proteins, the workhorses of every cell), but apparently non-functional DNA. This large non-genic fraction is mostly made up of remnants of "retrotransposons", which are sequences that are capable of copying and re-inserting themselves into the genome. In effect, retrotransposons are "selfish DNA", and they can have large effects on the structure and evolution of a genome. Is selfish DNA beneficial or harmful? Could it help plants adapt to new challenges such as new diseases? This study describes the retrotransposon content of two large regions of the soybean and common bean genomes, totaling 3.7 million DNA bases. This region was chosen for study because it also contains important disease resistance genes: against bacterial blight and soybean mosaic virus in soybean, and anthracnose (a fungal disease) in bean. The study finds that most retrotransposons in these soybean regions are recent (having inserted in the last 500,000 years), and they are being removed more slowly than they they have been added. This means that the soybean genome is probably expanding rather than contracting. Retrotransposons are also abundant and active in common bean. The ongoing activity of retrotransposons in these important crops means that new DNA variation is being generated over time in breeding populations. In the regions studied, the retrotransposon structure has led to mis-copying of the DNA, which has generated new copies of disease resistance genes in both soybean and common bean. Thus, "selfish DNA" has arguably helped in these crops' fight against disease.

Technical Abstract: Retrotransposons and their remnants often constitute more than 50% of higher plant genomes and have had major impacts on genome structure. Although extensively studied in monocot crops such as maize and rice, the impact of retrotransposons on major dicot crop genomes is not well documented. Here we present an analysis of retrotransposons in soybean (Glycine max), a major US and world crop. Analysis of approximately 3.7 megabases (Mb) of soybean 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 homologous recombination between LTRs is not the predominant mechanism for removal of retrotransposon sequences in soybean. Analysis of paired LTR sequences uncovered a low frequency of deletions relative to point mutations, indicating that removal of retrotransposon sequences by illegitimate recombination is operating more slowly than in previously characterized plant species. Thirteen of the 45 intact elements inserted within the last 500,000 years. Combined with the relatively slow removal rate of retrotransposons, these data indicate that the soybean genome is currently expanding rather than contracting. Significantly, we identified three subfamilies of non-autonomous elements that appear to be actively replicating, suggesting that retrotransposition can be catalyzed in trans by autonomous elements elsewhere in the genome. Analysis of 1.6 Mb of genomic sequence from G. 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 0.66 Mb of genomic sequence from Phaseolus vulgaris (common bean). Thus, autonomous and non-autonomous retrotransposons appear to be both abundant and active in Glycine and Phaseolus. The impact of non-autonomous retrotransposon replication on genome size appears to be much greater than previously appreciated.