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Annu. Rev. Plant Biol. 2012.63:283-305. Downloaded from www.annualreviews.org by University of Minnesota - Twin Cities - Wilson Library on 05/07/12. For personal use only. translocated into the pericentromeric region of the chromosome. Between the two Gm genome regions, 77% of gene duplicates were retained. However, this high level of retention did not extend to NBS-LRRs, which existed as clusters in both genome regions, but with significant homoeolog-specific duplications and losses. The pericentromeric region was especially reduced in surviving NBS-LRRs. Clearly, NBS-LRR genes are subject to much higher levels of fractionation than other gene classes. Local duplications, deletions, and recombination are apparently acting preferentially on WGD-derived NBS-LRR clusters, with the pericentromeric NBS-LRR cluster experiencing much higher levels of fractionation. This pattern has been noted in other plant species, with NBS-LRRs frequently underrepresented in duplicated genome regions (14, 64), potentially reflecting a fitness cost associated with excess NBS-LRRs (58). In a similar study by Kim et al. (44), a different pair of homoeologous genome regions (1.96–4.60 Mb) on Gm05 and Gm17 and centeredaroundtheRxp bacterial leaf pustule– resistance gene were examined and compared with the homologous Mt genome regions. In this case, fractionation in Mt was observed to extend to the level of gene blocks (in which multiple linked genes were retained in one duplicate) but lost from the other (contrasting with the apparent gene-by-gene fractionation illustrated in Figure 3). In the case of Gm and the more recent 13-Mya WGD, duplicates were also retained as blocks rather than individual genes, though some of the gene blocks were not lost, but were instead translocated to a different location in the Gm genome. Notably, the locations of homoeologs coincided with known QTLs for leaf pustule resistance, leading the authors to suggest that duplicated resistance genes may have retrained their ancestral function and then diverged in a pathogen strain–specific manner. Finally, Lin et al. (54) examined two ∼1-Mb homoeologous regions containing NBS-LRR clusters in Gm (on Gm08 and Gm15) as well as the orthologous region of common bean (P. vulgaris). The level of gene retention varied from 81% to 91% among the Gm segments, values somewhat higher than observed by others (39, 44; Figure 3). As in Innes et al. (39), this analysis uncovered significant differences in retrotransposon density between the two regions, differences that were correlated with differing levels of structural variation. Going beyond structural analysis, the study examined gene expression levels along the two Gm segments and found 38% higher transcriptional activity on Gm08 compared with Gm15 based on a metric that integrated expression among seven different tissues. This difference in expression activity is significant because expression variation between retained gene pairs is an expectation of sub- and neofunctionalization. Genome Duplication and the Evolution of Nodulation The property most striking about legumes is their capacity to form symbiotic nitrogen-fixing nodules in association with rhizobial bacteria. Not surprisingly, detailed analysis of legume genomes can provide valuable insights into symbiosis, nodulation, and nitrogen fixation. At the simplest level, genome sequence data make it possible to generate a global inventory of nodulation-related genes. This was an important contribution of the recent Gm sequence (91). Here, genes of interest were identified by searching for Gm genes orthologous to known nodulation-related genes in any legume species. As a result, 34 Gm nodulins (noduleupregulated proteins) were discovered along with 23 nodulation-related regulatory genes within the Gm genome. This kind of gene inventory makes it possible to explore local nodulation-related gene clusters, putative homoeologs, and membership in related gene families. This inventory should be especially valuable in dissecting the global regulatory machinery controlling plant-rhizobium communication and nodule development. Analysis of the Mt genome sequence focused on the relationship between genome duplication and the evolution of nodulation. 298 Young·Bharti
Annu. Rev. Plant Biol. 2012.63:283-305. Downloaded from www.annualreviews.org by University of Minnesota - Twin Cities - Wilson Library on 05/07/12. For personal use only. Previous studies had established that legumes belong to a clade of rosids, Fabidae, that all share a predisposition to nodulate, presumably derived from their common ancestor (88). In analyzing the Mt genome, the question was whether the 58-Mya WGD contributed in any way to the elaboration of rhizobial nodulation. The answer appears to be a qualified yes. Multiple lines of evidence indicate that nodulation machinery predates the 58-Mya WGD. Moreover, many of the known regulatory steps in rhizobial nodulation are shared with mycorrhizal signaling (66), a symbiosis broadly shared among angiosperms (9). Just a few of the known recognition steps are exclusively associated with rhizobial nodulation, including the key receptor-like kinase, NFP (66). In analyzing the Mt genome, NFP was found to have a homoeolog, LYR1, and genome position and K s data indicate that these duplicated genes derive from the 58-Mya WGD. NFP is nodulation specific in expression and function, whereas LYR1 is upregulated in mycorrhizae (30). In separate work, a nodulating nonlegume, Parasponia andersonii, is known to contain a single gene coding for a protein with the functions of both NFP and LYR1 (68). Therefore, one likely interpretation would be that the 58-Mya papilionoid WGD led to subfunctionalization of a more ancient gene that previously carried out both functions, resulting in two descendent genes that split the nodulation and mycorrhizal recognition functions between them. A separate nodulation-related transcription factor, ERN1 (96), also possesses a homoeolog (ERN2) in Mt. Like NFP/LYR1, ERN1 and ERN2 have contrasting nodulation-versus-mycorrhizal expression patterns and also derive from the 58-Mya WGD. Potentially, they are a second example of sub- or neofunctionalization resulting from the papilionoid WGD event. These observations even suggest a potential phylogenetic strategy for discovering genes that play a role in nodulation. It should be possible to mine the products of the 58-Mya WGD and search for genes that have nodulerelated expression in one or both gene products of the WGD event. At this point, one could examine potentially novel (or at least interesting) functions that these genes might be playing in nodulation. Indeed, this strategy has already been put into practice with the identification of a cytokinin response regulator promoting the expression of ERN1 (67). Analysis of the Mt genome uncovers 51 additional WGDderived homoeolog pairs with one or both duplicates upregulated in nodules, including 10 additional transcription factor genes. PERSPECTIVES ON LEGUME GENOMICS It is difficult to believe that massive amounts of sequence data have been available in plants for such a short time. The pace of change has been so rapid that in less than a decade we have gone from having only thousands of ESTs in a few legume species to having three robust legume reference genomes. This review has examined ways in which the rapidly growing body of genome sequence data sheds light on legume biology. At the simplest level, translation of genome data between legume species enables important practical applications: the discovery of genetic markers, the development of linkage maps, and the saturation of genome regions for positional cloning. This is especially true for minor legumes, where many species are important to agriculture but supported by small research communities. At a more basic level, dissection of genome sequence data reveals the structure, architecture, and evolution of important gene families and enables the identification of orthologous versus paralogous relationships. Complete genome sequences also reveal legume- and species-specific genes whose functions remain largely unknown, although unquestionably important. Gene and genome duplications, so critical in shaping plant genomes, contain intrinsic information that can be exploited to predict function and the structure of genetic networks. Candidate gene discovery based on the papilionoid WGD is a promising example. In legumes, applying these strategies to nodulation and seed development will be especially critical. Additional www.annualreviews.org • Genome-Enabled Insights into Legume Biology 299
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