Bridging Model and Crop Legumes through Comparative Genomics

Abstract

The Fabaceae, or legumes, constitute the third largest family of flowering plants, comprising more than 650 genera and 18,000 species (Polhill and Raven, 1981). Economically, legumes represent the second most important family of crop plants after Poaceae (grass family), accounting for approximately 27% of the world's crop production (Graham and Vance, 2003). On a worldwide basis, legumes contribute about one-third of humankind's protein intake, while also serving as an important source of fodder and forage for animals and of edible and industrial oils. One of the most important attributes of legumes is their unique capacity for symbiotic nitrogen fixation, underlying their importance as a source of nitrogen in both natural and agricultural ecosystems. Legumes also accumulate natural products (secondary metabolites) such as isoflavonoids that are beneficial to human health through anticancer and other health-promoting activities (Dixon and Sumner, 2003). Dendrogram depicting phylogenetic relationships of Papilionoideae legumes. (Figure reprinted from Choi et al. [2004b], based on figure 5 of Doyle and Luckow [2003].) Chromosome number and genome size of major model and crop legumesa Data were from the Plant DNA C-values Database (http://www.rbgkew.org.uk/cval/homepage.html). Chromosome number and genome size of major model and crop legumesa Data were from the Plant DNA C-values Database (http://www.rbgkew.org.uk/cval/homepage.html). An immediate goal of legume genomics is to transfer knowledge between model and crop legumes. Accordingly, an in-depth understanding of conservation of genome structure among legume species is a prerequisite to achieving this goal. The idea that conserved genome structure can facilitate transfer of knowledge among related plant species is best addressed in grasses in which genome macrosynteny and microsynteny have been extensively maintained (Bennetzen, 2000; Devos and Gale, 2000). These studies, however, also revealed many exceptions to the conserved synteny, with frequent local genic rearrangements including gene inversion, duplication, translocation, and insertion/deletion. Although the degeneracy of local genome microstructure has been widely documented, it is less clear the extent to which such alterations to genome microstructure contribute to the divergence of genome function. In this review, we focus on recent results of comparative genome analysis between model and crop legumes, and also highlight the recent successes of using comparative genomics tools for cross-species gene isolation. It has been estimated that upwards of 80% of all angiosperms are likely to have a polyploid origin (Masterson, 1994). It is unlikely that legumes are an exception to this. Soybean, for example, has long been known to be an ancient polyploid with putative homoeologous chromosomal regions readily identified by genetic mapping (Shoemaker et al., 1996; Lee et al., 1999, 2001) and by characterization of homoeologous bacterial artificial chromosome (BAC) clones (Foster-Hartnett et al., 2002; Yan et al., 2003). And recently, segmental duplications within the soybean genome were visualized by fluorescence in situ hybridization of BACs (Pagel et al., 2004). Segmental duplications also were identified in the M. truncatula and L. japonicus genomes through high-throughput genome sequencing (Zhu et al., 2003; N. Young, personal communication). Extensive expressed sequence tag (EST) collections exist for two legumes representing distinct phylogenetic clades, soybean (tropical legumes) and M. truncatula (cool season legumes). Much of a genome's evolutionary history can be read in these transcripts. Schlueter et al. (2004) identified duplicate transcripts from the EST collections of both of these legumes and estimated genetic distances of the pairs using synonymous substitution measurements. It was estimated that soybean probably underwent two major genome duplications events: one at 15 million years ago (MYA) and another at 44 MYA. A genome duplication event also was estimated to have occurred in M. truncatula at approximately 58 MYA. A subsequent analysis using a multigene approach concluded that the more ancient duplication events probably represent a single event that occurred before soybean and Medicago diverged (Pfeil et al., 2005). If this is true, then approximately 7,000 other legumes share the same genome duplication event (Pfeil et al., 2005). Genome duplications often are followed by gene loss, rearrangements, tandem gene or segmental duplications, and divergence of duplicated gene sequences. All of these events are involved in the process of diploidization (Ohno, 1970) and complicate the interpretation of comparative genomic data. Macrosynteny generally refers to conserved gene order between species revealed by comparative genetic mapping of common DNA markers or in silico mapping of homologous sequences. Early comparative studies of legume genomes were focused on closely related species of