Differential Accumulation of Retroelements and Diversification of NB-LRR Disease Resistance Genes in Duplicated Regions Following Polyploidy in the Ancestor of Soybean

Authors: INNES, ROGER - INDIANA UNIV; AMELINE-TORREGROSA, CARINE - UNIV MINNESOTA-ST. PAUL; ASHFIELD, TOM - INDIANA UNIV; CANNON, ETHALINDA - ISU; Cannon, Steven; CHACKO, BEN - UNIV MINNESOTA-ST. PAUL; CHEN, NICOLAS - INRA, ORSAY, FRANCE; COULOUX, ARNAUD - CNS, EVRY, FRANCE; DALVANI, ANITA - INDIANA UNIV; DENNY, ROXANNE - UNIV MINNESOTA-ST. PAUL; DESHPADE, SHWETA - UNIV OKLAHOMA; DOYLE, JEFF - CORNELL UNIV; EGAN, ASHLEY - CORNELL UNIV; GEFFROY, VALERIE - INRA, ORSAY, FRANCE; GLOVER, NATASHA - VIRGINIA TECH; HANS, CHRISTIAN - PURDUE UNIV; HOWELL, STACY - INDIANA UNIV; ILUT, DAN - CORNELL UNIV; JACKSON, SCOTT - PURDUE UNIV; LAI, HONGSHING - UNIV OKLAHOMA; MAMMADOV, JAFAR - VIRGINIA TECH; MARTIN DEL CAMPO, SARA - INDIANA UNIV; METCALF, MICHELLE - INDIANA UNIV; NGUYEN, ASHLEY - VIRGINIA TECH; O'BLENESS, MAJESTA - UNIV OKLAHOMA; PFEIL, BERNARD - CORNELL UNIV; PODICHETI, RAM - INDIANA UNIV; RATNAPARKHE, MILIND - VIRGINIA TECH; ROE, BRUCE - UNIV OKLAHOMA; SAGHAI, M - VIRGINIA TECH; SAMAIN, SYLVIE - CNS, EVRY, FRANCE; SANDERS, IRYNA - UNIV OKLAHOMA; SEGURENS, BEATRICE - CNS, ENRY, FRANCE; SEVIGNA, MIREILLE - INRA, ORSAY, FRANCE; SHERMAN-BROYLES, SUE - CORNELL UNIV; THAREAU, VINCENT - CNRS, ORSAY, FRANCY; TUCKER, DOMINIC - VIRGINIA TECH; WALLING, JASON - PURDUE UNIV; WAWRZYNSKI, ADAM - INDIANA UNIV; YI, JING - CNS, ENVRY, FRANCE; YOUNG, NEVIN - UNIV MINNESOTA

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/6/2008
Publication Date: 10/8/2008
Citation: Innes, R.W., Ameline-Torregrosa, C., Ashfield, T., Cannon, E., Cannon, S.B., Chacko, B., Chen, N.W., Couloux, A., Dalvani, A., Denny, R., Deshpade, S., Doyle, J.J., Egan, A., Geffroy, V., Glover, N., Hans, C.S., Howell, S., Ilut, D., Jackson, S., Lai, H., Mammadov, J., Martin Del Campo, S., Metcalf, M., Nguyen, A., O'Bleness, M., Pfeil, B., Podicheti, R., Ratnaparkhe, M., Roe, B., Saghai, M.A., Samain, S., Sanders, I., Segurens, B., Sevigna, M., Sherman-Broyles, S., Thareau, V., Tucker, D., Walling, J., Wawrzynski, A., Yi, J., Young, N.D. 2008. Differential Accumulation of Retroelements and Diversification of NB-LRR Disease Resistance Genes in Duplicated Regions Following Polyploidy in the Ancestor of Soybean. Plant Physiology. 148:1740-1759.

Interpretive Summary: Although plants and animals both have basically the same genetic structure (DNA in chromosomes, containing the blueprint for the entire organism), plants have an intriguing difference. The genomes of most, if not all, flowering plants appear to have undergone whole genome duplication events multiple times during the course of their evolution. Whole genome duplication has occurred shortly before or during the domestication of most crop plants, so it is probably important in creating new traits that humans can mold through selective breeding. The impact of genome duplication is poorly understood however. This study examined approximately one million letters of DNA from soybean, in a region rich with disease-resistance genes, and the corresponding portion from the duplicated region (following a genome duplication at about 12 million years ago). Then, to track DNA and gene changes over time, the study examined the corresponding sequence from a set of increasingly distant species: from another variety of soybean, then from a moderately-close wild relative, then from common bean (which separated about 20 million years ago), and finally from a relative of alfalfa (which separated about 50 million years ago). This cross section over time shows how genes and associated biological traits have changed. A group of genes that guards against the soybean diseases "bacterial blight" and "soybean mosaic virus" has expanded in soybean, but only in one of the chromosome copies. In the duplicated chromosome, most of these genes have been lost, and the chromosome region has expanded with apparently non-functional DNA. Thus, this important group of disease resistance genes has evolved by gaining copies on one chromosome, and losing copies on the other. Meanwhile, in common bean, disease resistance genes have also increased in number, and one has acquired the role of defense against anthracnose (a serious fungal disease in bean). Taken together, the study describes how several plant species have changed after genome duplications, and how disease resistance genes in particular respond to evolving pathogens and to the changing conditions in the plant genomes.

Technical Abstract: The genomes of most flowering plants have undergone polyploidization at some point in their evolution. How such polyploidization events have impacted the subsequent evolution of genome structure is poorly understood. We sequenced two homoeologous regions in soybean (Glycine max), which underwent a polyploidy event 10-14 million years ago (mya), and the orthologous/homoeologous regions in several related legumes (a second G. max genotype, G. tomentella, Phaseolus vulgaris and Medicago truncatula). The Phaseolus and Medicago genomes lack this polyploidy event, enabling us to determine the origin of differences between Glycine homologues. Comparison of the two G. max homoeologues revealed that the majority of low-copy genes (78%) have been retained in both homoeologues following polyploidization. In contrast, nucleotide binding-leucine rich repeat disease resistance gene clusters have undergone dramatic species/homoeologue-specific expansions, with some evidence for partitioning of subfamilies between homoeologues. The biggest difference between homoeologues, however, was in retroelement content, with homoeologue 2 (H2) having expanded to three times the size of homoeologue 1 (H1) due to retroelement insertions. Fluorescent in situ hybridization revealed that the H2 region was located near a centromere. The pericentromeric location correlated with a higher frequency of low copy gene loss from H2. However, low copy genes on H2 are under purifying selection and are evolving at the same rate as those on H1. One of the duplicated regions in soybean accumulated vast numbers of repetitive DNA elements known as retroelements, which can cause gene disruptions and gene silencing. Despite this accumulation of retroelements, over 75% of the low-copy duplicated genes in this region have been retained in the same order and continue to function. This finding contrasts with recent analyses of the maize genome, in which only about a third of duplicated genes appear to have been retained over a similar time period. The fate of the disease resistance genes was different, however. These have expanded in H1 but mostly been lost from H2. A proposed mechanism for this differential expansion and loss is that suppressed recombination in the pericentromere in H2 has suppressed gene "births" seen in the tandem clusters of resistance genes in H1.