We used nine complete genome sequences, from grape, poplar, Arabidopsis, soybean, lotus, apple, strawberry, cacao, and papaya, to investigate the paleohistory of rosid crops. We characterized an ancestral rosid karyotype, structured into 7/21 protochomosomes, with a minimal set of 6,250 ordered protogenes and a minimum physical coding gene space of 50 megabases. We also proposed ancestral karyotypes for the Caricaceae, Brassicaceae, Malvaceae, Fabaceae, Rosaceae, Salicaceae, and Vitaceae families with 9, 8, 10, 6, 12, 9, 12, and 19 protochromosomes, respectively. On the basis of these ancestral karyotypes and present-day species comparisons, we proposed a two-step evolutionary scenario based on allohexaploidization involving the newly characterized A, B, and C diploid progenitors leading to dominant (stable) and sensitive (plastic) genomic compartments in any modern rosid crops. Finally, a new user-friendly online tool, “DicotSyntenyViewer” (available from http://urgi.versailles.inra.fr/synteny-dicot), has been made available for accurate translational genomics in rosids.

Since the availability of assembled eukaryotic genomes, the first one being a budding yeast, many computational methods for the reconstruction of ancestral karyotypes and gene orders have been developed. The difficulty has always been to assess their reliability, since we often miss a good knowledge of the true ancestral genomes to compare their results to, as well as a good knowledge of the evolutionary mechanisms to test them on realistic simulated data. In this study, we propose some measures of reliability of several kinds of methods, and apply them to infer and analyse the architectures of two ancestral yeast genomes, based on the sequence of seven assembled extant ones. The pre-duplication common ancestor of S. cerevisiae and C. glabrata has been inferred manually by Gordon et al. (Plos Genet. 2009). We show why, in this case, a good convergence of the methods is explained by some properties of the data, and why results are reliable. In another study, Jean et al. (J. Comput Biol. 2009) proposed an ancestral architecture of the last common ancestor of S. kluyveri, K. thermotolerans, K. lactis, A. gossypii, and Z. rouxii inferred by a computational method. In this case, we show that the dataset does not seem to contain enough information to infer a reliable architecture, and we construct a higher resolution dataset which gives a good reliability on a new ancestral configuration.

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Motivation: Ancestral genomes provide a better way to understand the structural evolution of genomes than the simple comparison of extant genomes. Most ancestral genome reconstruction methods rely on universal markers, that is, homologous families of DNA segments present in exactly one exemplar in every considered species. Complex histories of genes or other markers, undergoing duplications and losses, are rarely taken into account. It follows that some ancestors are inaccessible by these methods, such as the proto–monocotyledon whose evolution involved massive gene loss following a whole genome duplication.Results: We propose a mapping approach based on the combinatorial notion of ‘sandwich consecutive ones matrix’, which explicitly takes gene losses into account. We introduce combinatorial optimization problems related to this concept, and propose a heuristic solver and a lower bound on the optimal solution. We use these results to propose a configuration for the proto-chromosomes of the monocot ancestor, and study the accuracy of this configuration. We also use our method to reconstruct the ancestral boreoeutherian genomes, which illustrates that the framework we propose is not specific to plant paleogenomics but is adapted to reconstruct any ancestral genome from extant genomes with heterogeneous marker content.Availability: Upon request to the authors.Contact: haris.gavranovic@gmail.com; eric.tannier@inria.fr