Abstract
BackgroundMany metazoan genomes conserve chromosome-scale gene linkage relationships (“macro-synteny”) from the common ancestor of multicellular animal life [1-4], but the biological explanation for this conservation is still unknown. Double cut and join (DCJ) is a simple, well-studied model of neutral genome evolution amenable to both simulation and mathematical analysis [5], but as we show here, it is not sufficent to explain long-term macro-synteny conservation.ResultsWe examine a family of simple (one-parameter) extensions of DCJ to identify models and choices of parameters consistent with the levels of macro- and micro-synteny conservation observed among animal genomes. Our software implements a flexible strategy for incorporating genomic context into the DCJ model to incorporate various types of genomic context (“DCJ-[C]”), and is available as open source software from http://github.com/putnamlab/dcj-c.ConclusionsA simple model of genome evolution, in which DCJ moves are allowed only if they maintain chromosomal linkage among a set of constrained genes, can simultaneously account for the level of macro-synteny conservation and for correlated conservation among multiple pairs of species. Simulations under this model indicate that a constraint on approximately 7% of metazoan genes is sufficient to constrain genome rearrangement to an average rate of 25 inversions and 1.7 translocations per million years.
Highlights
Many metazoan genomes conserve chromosome-scale gene linkage relationships (“macro-synteny”) from the common ancestor of multicellular animal life [1,2,3,4], but the biological explanation for this conservation is still unknown
Our software includes a modified binary search tree with “reverse” flags and subtree summaries on nodes so that all the information necessary to carry out Double cut and join (DCJ)-[C] operations, such as counting “sensitive” genes on any fragment, can be completed in O(log N) time. [11,12,13] we do not enforce balanced binary trees for a strict bound on performance, we found chromosome gene trees to remain O(log N) height on average, with correspondingly fast running time. (Data not shown.) The software can be downloaded from http://github.com/putnamlab/dcj-c
This study shows that the DCJ model of genome evolution can be extended to generate simple models sufficient to explain the observed levels of micro- and macro-synteny conservation, by directly limiting the size and/or frequency of inter-chromosomal rearrangements, or by constraining the movement between chromosomes of a small fraction of genes
Summary
Many metazoan genomes conserve chromosome-scale gene linkage relationships (“macro-synteny”) from the common ancestor of multicellular animal life [1,2,3,4], but the biological explanation for this conservation is still unknown. Indirect methods have been developed [1,2] to infer chromosome-scale linkage from orthologous genes shared between scaffolds of different draft genome assemblies. We apply those methods here to partition the scaffolds (or chromosome segments, in the case of the human genome) of five metazoan genomes by biclustering. The scaffolds in each group share a distinct distribution of orthologs across the groups of other genomes. This pattern is clearly visible in the human-piacozoan “dot plot” of Figure 1a
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