Polyploidy Did Not Predate the Evolution of Nodulation in All Legumes

United States Department of Agriculture-Agricultural Research Service, Corn Insects and Crop Genomics Research Unit, Iowa State University, Ames, Iowa, United States of America.
PLoS ONE (Impact Factor: 3.23). 07/2010; 5(7):e11630. DOI: 10.1371/journal.pone.0011630
Source: PubMed


Several lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has not been known whether this event was confined to the papilionoid subfamily (Papilionoideae; e.g. beans, medics, lupins) or occurred earlier. Determining the timing of the polyploidy event is important for understanding whether polyploidy might have contributed to rapid diversification and radiation of the legumes near the origin of the family; and whether polyploidy might have provided genetic material that enabled the evolution of a novel organ, the nitrogen-fixing nodule. Although symbioses with nitrogen-fixing partners have evolved in several lineages in the rosid I clade, nodules are widespread only in legume taxa, being nearly universal in the papilionoids and in the mimosoid subfamily (e.g., mimosas, acacias)--which diverged from the papilionoid legumes around 58 million years ago, soon after the origin of the legumes.
Using transcriptome sequence data from Chamaecrista fasciculata, a nodulating member of the mimosoid clade, we tested whether this species underwent polyploidy within the timeframe of legume diversification. Analysis of gene family branching orders and synonymous-site divergence data from C. fasciculata, Glycine max (soybean), Medicago truncatula, and Vitis vinifera (grape; an outgroup to the rosid taxa) establish that the polyploidy event known from soybean and Medicago occurred after the separation of the mimosoid and papilionoid clades, and at or shortly before the Papilionoideae radiation.
The ancestral legume genome was not fundamentally polyploid. Moreover, because there has not been an independent instance of polyploidy in the Chamaecrista lineage there is no necessary connection between polyploidy and nodulation in legumes. Chamaecrista may serve as a useful model in the legumes that lacks a paleopolyploid history, at least relative to the widely studied papilionoid models.

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    • "Parasponia diverged somewhere between 100 and 120 Ma from the papilionoids [46], whereas Chamaecrista diverged approximately 60 Ma from the papilionoids [45]. Independent of whether their last common ancestor could already perform nodulation or whether this trait evolved independently in both lineages, this would suggest that the ability for advanced nodulation characteristics was not able to evolve for about 40–60 Ma, whereas it did so very rapidly after the papilionoid WGD [45]. This emphasizes that although the papilionoid WGD was not an absolute prerequisite for the evolution of nitrogen-fixing nodulation, it most likely facilitated the development of several elaborate papilionoid nodule forms. "
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    • "Recently, comparisons between legume genomes have revealed that legumes of the large Papilionoideae subfamily (papilionoids) have undergone whole-genome duplication [5]. This older shared polyploidy event is estimated to have occurred 56 to 65 million years ago (Mya) [6], [7]. A second, more recent genome duplication event occurred only in the lineage leading to Glycine up to 13 Mya [8]. "
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    PLoS ONE 07/2014; 9(7):e102825. DOI:10.1371/journal.pone.0102825 · 3.23 Impact Factor
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    • "soja), both annual species native to northeastern Asia, as well as approximately 30 perennial species native to Australia classified as subgenus Glycine (Ratnaparkhe, Singh & Doyle, 2011). Like many plant species, Glycine has a complex history of polyploidy: in addition to events shared with all angiosperms (Jiao et al., 2011) and eudicots (Jiao et al., 2012), the soybean genome retains evidence from a WGD around 50 million years ago (MYA) shared with a large subset of legumes (Blanc & Wolfe, 2004; Schlueter et al., 2004; Cannon et al., 2010), and particularly from a more recent polyploidy event that increased the chromosome number of the ancestor of all extant Glycine species from 2n = 20 to 2n = 40 (Shoemaker, Schlueter & Doyle, 2006; Doyle & Egan, 2010; Schmutz et al., 2010; Doyle, 2012). This Glycine-specific WGD occurred between the estimated time of homoeologous gene divergence in the soybean genome (10–13 MYA; e.g., Egan & Doyle, 2010; Schmutz et al., 2010), and around 5 MYA, when the annual and perennial species diverged from an already-polyploid common ancestor (Doyle & Egan, 2010). "
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