Locating Multiple Gene Duplications through Reconciled Trees

The analysis of the first plant genomes provided unexpected evidence for genome duplication events in species that had previously been considered as true diploids on the basis of their genetics. These polyploidization events may have had important consequences in plant evolution, in particular for species radiation and adaptation and for the modulation of functional capacities. Here we report a high-quality draft of the genome sequence of grapevine (Vitis vinifera) obtained from a highly homozygous genotype. The draft sequence of the grapevine genome is the fourth one produced so far for flowering plants, the second for a woody species and the first for a fruit crop (cultivated for both fruit and beverage). Grapevine was selected because of its important place in the cultural heritage of humanity beginning during the Neolithic period. Several large expansions of gene families with roles in aromatic features are observed. The grapevine genome has not undergone recent genome duplication, thus enabling the discovery of ancestral traits and features of the genetic organization of flowering plants. This analysis reveals the contribution of three ancestral genomes to the grapevine haploid content. This ancestral arrangement is common to many dicotyledonous plants but is absent from the genome of rice, which is a monocotyledon. Furthermore, we explain the chronology of previously described whole-genome duplication events in the evolution of flowering plants.

Gene duplication has generally been viewed as a necessary source of material for the origin of evolutionary novelties, but it is unclear how often gene duplicates arise and how frequently they evolve new functions. Observations from the genomic databases for several eukaryotic species suggest that duplicate genes arise at a very high rate, on average 0.01 per gene per million years. Most duplicated genes experience a brief period of relaxed selection early in their history, with a moderate fraction of them evolving in an effectively neutral manner during this period. However, the vast majority of gene duplicates are silenced within a few million years, with the few survivors subsequently experiencing strong purifying selection. Although duplicate genes may only rarely evolve new functions, the stochastic silencing of such genes may play a significant role in the passive origin of new species.

Integration of structural genomic data from a largely assembled rice genome sequence, with phylogenetic analysis of sequence samples for many other taxa, suggests that a polyploidization event occurred approximately 70 million years ago, before the divergence of the major cereals from one another but after the divergence of the Poales from the Liliales and Zingiberales. Ancient polyploidization and subsequent "diploidization" (loss) of many duplicated gene copies has thus shaped the genomes of all Poaceae cereal, forage, and biomass crops. The Poaceae appear to have evolved as separate lineages for approximately 50 million years, or two-thirds of the time since the duplication event. Chromosomes that are predicted to be homoeologs resulting from this ancient duplication event account for a disproportionate share of incongruent loci found by comparison of the rice sequence to a detailed sorghum sequence-tagged site-based genetic map. Differential gene loss during diploidization may have contributed many of these incongruities. Such predicted homoeologs also account for a disproportionate share of duplicated sorghum loci, further supporting the hypothesis that the polyploidization event was common to sorghum and rice. Comparative gene orders along paleo-homoeologous chromosomal segments provide a means to make phylogenetic inferences about chromosome structural rearrangements that differentiate among the grasses. Superimposition of the timing of major duplication events on taxonomic relationships leads to improved understanding of comparative gene orders, enhancing the value of data from botanical models for crop improvement and for further exploration of genomic biodiversity. Additional ancient duplication events probably remain to be discovered in other angiosperm lineages.