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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. Here, chromosome arms for both Mt and Lj (based on the estimated positions of centromeric regions) have been reordered and in some cases flipped (noted by an asterisk) to align synteny blocks into a single coherent line. The result highlights the genome-scale synteny observed between the two species. If perfect synteny existed between Mt and Lj, the roughly 45 ◦ dot-plot line would be straight and continuous, and would reach all the way from one end to the other. The fact that the actual result produces a line that approaches this ideal is overwhelming evidence for genome-scale synteny between the two species. Synteny blocks are nearly the lengths of whole chromosome arms, and overall they span more than 75% of both species. One striking example between Mt05N and Lj02S is circled in red. Still, there are also breaks in synteny—for example, Mt07S and its synteny with Lj01S (circled in green). Here, rather than a contiguous diagonal line, one sees a cloud of shorter synteny blocks, broken into six pieces with two of them flipped around. Apparently, one or both syntenic chromosomes experienced major reorganization events since the separation of Mt and Lj.Therearealsonotable genome regions where synteny is totally lacking between the two species. Mt06N with Lj06S and Mt03N/Mt04N with Lj03N (circled in purple) are striking examples. Significantly, these genome regions coincide with higher densities of NBS-LRRs and retrotransposons compared with the remainder of the genome, a relationship that may be biologically significant (5) and similar in terms of degraded synteny to observations made in A. hypogaea (76). Envisioning the Ancestral Legume Genome Inevitably, as more legumes are sequenced it will become possible to reconstruct the ancestral legume genome, or at least the ancestral papilionoid genome. Such an effort is underway by integrating the sequenced legume genomes with comparably high-density marker/map data from species such as chickpea (C. arietinum) and pigeon pea (C. cajan) (D. Cook, personal communication). Comparisons of the Gm, Mt, and Lj genomes already provide a glimpse into the large-scale architecture of the ancestral legume genome. Despite the complexities resulting from the 13-Mya Glycine WGD event (discussed in further detail below), comparisons among Gm, Mt,andLj (Figures 1 and 2) suggest a limited number of ancestral synteny blocks that have been rearranged to generate present-day papilionoid genomes. In both comparisons, a conservative examination reveals just 14 largely coherent blocks that span the majority of all three genomes. Notably, this estimate agrees nicely with the apparent basal chromosome number of seven for papilionoids (74). GENOME DUPLICATIONS IN LEGUME BIOLOGY Whole-Genome Duplication Events in the History of Legumes One of the most striking lessons coming out of plant comparative genomics has been the critical role of genome duplication in the evolutionary history of many, if not most, plant species (21). This is especially true in the case of legumes. Gm provided an early hint into the importance of WGD in genome restructuring in a study showing that restriction fragment length polymorphisms were duplicated on average 2.55 times and localized to a homoeologous segment (paralogous sequences resulting from WGD) nearly as long as whole chromosomes (84). Later, as large amounts of genome sequence data became available, it became clear that most present-day plant genomes are the products of ancient genome-scale duplication events (examples include 3, 40, 41, 91). Subsequent studies have gone on to reveal the wide range of plant families that have experienced genome duplications and the architecture of retained duplication blocks, and have established reasonably precise estimates for the timing of key duplication events (7, 73, 85). We know, for example, that many dicots share an ancient (130–140 Mya) triploidization event based on 294 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. synteny analysis of Vitus vinifera and the fact that each Vitus region typically shows synteny to three corresponding regions in other sequenced dicots (41). We also know that a surprisingly large number of plant WGD events followed closely after the Cretaceous-Tertiary boundary event ∼65 Mya. This led Fawcett et al. (22) to suggest that polyploids might have higher adaptability and greater tolerance to extreme conditions, something that would have come in quite handy during a time of widespread species extinction. Finally, we are beginning to discover the details about the aftermath of WGD events (summarized in 24)—and it is this final point, the consequence of genome duplication, that is especially relevant to our consideration of legume genome biology. Genome duplication is easy to see when looking at a dot-plot comparison. A closer look at Figure 1 reveals numerous secondary synteny blocks lying to one side or the other of the main diagonal. One notable example is where the primary synteny block involving Mt01N and Lj05N is paralleled by another synteny block lower down, between Mt01N and Lj01N (orange circles connected by an orange line). There are dozens of such duplicated synteny blocks in the comparison between these two species, and the simplest interpretation is an ancient WGD preceding the speciation between Mt and Lj. In a comparison like this, synteny blocks lying along the main diagonal represent the speciation event, whereas the off-center diagonals show regions of synteny resulting from one or more shared WGD events. Apparently, a WGD event that took place in the ancestor of Mt and Lj was followed quickly by a period of significant genome rearrangement and gene loss before speciation, rapidly degrading the quality of duplicate synteny blocks observed. (Loss of synteny in duplicate blocks is important in understanding the impact of duplication on legume biology and is discussed in more detail below.) The existence of such a WGD in the legume family has been indicated through multiple sources of evidence, especially K s (synonymous substitution) estimates between paralogs (6, 73, 80) and topology of phylogenetic tree analysis (12, 15). Integrating all these different sources of data leads to a best estimate for the timing of this WGD of 58 Mya. This date would have preceded the Mt/Lj split (approximately 50 Mya) as well as the split with Gm (54 Mya) (52). Indeed, peanut (A. hypogaea), an earlier diverging papilionoid, also shares this WGD event (5). By contrast, a recent study in Chamaecrista indicates that this species (and presumably the Mimosoideae and Caesalpinioideae subfamilies) do not share the 58-Mya WGD event (12). In other words, we know with remarkable precision both the timing and evolutionary window for this pivotal WGD event in the history of legumes. Given the range of species that share this duplication, we will refer to it as the papilionoid WGD. But the papilionoid WGD is not the only one to play an important role in legume evolution. Figure 2 displays a comparison of the Mt and Gm genome sequences (based on their recently published sequences). This comparison illustrates important similarities but also striking differences with the Mt/Lj dot-plot in Figure 1. Gm and Mt clearly display extensive synteny, with many long, coherent synteny blocks. A quick count reveals as many as 30 large-scale synteny blocks running the length of chromosome arms or nearly so. However, there is not a single 45 ◦ diagonal stretching across the genomes; instead, there are pairs of diagonals in Gm corresponding to individual chromosome arms of Mt. One example (circled in red) highlights synteny between Mt05S and two different Gm chromosomes/arms, Gm02S and Gm14N/Gm14S. A WGD is again the explanation, but this time, one that occurred more recently (estimated at 13 Mya) and only in the lineage leading to Gm (84). This duplication event explains the observation that there are two Gm blocks for each Mt genome region. Comparable levels of contiguity observed in each pair of synteny blocks are explained by the fact that both trace back to a single WGD event, and so the evolutionary distance between Mt and both of the Gm syntenic segments must be identical. This Glycine-specific WGD had been predicted previously (84), but the publication www.annualreviews.org • Genome-Enabled Insights into Legume Biology 295
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