Comparative analysis of chicken chromosome 28 provides new clues to the evolutionary fragility of gene-rich vertebrate regions

Abstract

The chicken genome draft sequence has provided a valuable resource for studies of an important agricultural and experimental model species and an important data set for comparative analysis. However, some of the most gene-rich segments are missing from chicken genome draft assemblies, limiting the analysis of a substantial number of genes and preventing a closer look at regions that are especially prone to syntenic rearrangements. To facilitate the functional and evolutionary analysis of one especially gene-rich, rearrangement-prone genomic region, we analyzed sequence from BAC clones spanning chicken microchromosome GGA28; as a complement we also analyzed a gene-sparse, stable region from GGA11. In these two regions we documented the conservation and lineage-specific gain and loss of protein-coding genes and precisely mapped the locations of 31 major human-chicken syntenic breakpoints. Altogether, we identified 72 lineage-specific genes, many of which are found at or near syntenic breaks, implicating evolutionary breakpoint regions as major sites of genetic innovation and change. Twenty-two of the 31 breakpoint regions have been reused repeatedly as rearrangement breakpoints in vertebrate evolution. Compared with stable GC-matched regions, GGA28 is highly enriched in CpG islands, as are break-prone intervals identified elsewhere in the chicken genome; evolutionary breakpoints are further enriched in GC content and CpG islands, highlighting a potential role for these features in genome instability. These data support the hypothesis that chromosome rearrangements have not occurred randomly over the course of vertebrate evolution but are focused preferentially within "fragile" regions with unusual DNA sequence characteristics.

A Gene-Based Genetic Linkage Map of the Collared Flycatcher (Ficedula albicollis) Reveals Extensive Synteny and Gene-Order Conservation During 100 Million Years of Avian Evolution

“…One possible explanation relates to the role of repeat elements in governing chromosome fragility and the dearth of active families of interspersed repeat elements in avian genomes (International Chicken Genome Sequencing Consortium 2004). Breakpoints for chromosome rearrangements tend to be enriched with interspersed repetitive elements, low-copy repeats, and segmental duplications (Bailey et al 2004;Freudenreich 2007;Kehrer-Sawatzki and Cooper 2007), including in chicken (Gordon et al 2007). Mechanistically, unequal crossing over between repeated sequences within or between chromosomes is likely to contribute to this pattern (Lupski and Stankiewicz 2005).…”

Finding and Comparing Syntenic Regions among Arabidopsis and the Outgroups Papaya, Poplar, and Grape: CoGe with Rosids

“…If noncollinear gene orders can be explained by chromosomal aberrations, then synteny may often be inferred. Single-gene transpositions obfuscate synteny, as do rearrangementprone regions (Fortna et al, 2004;Gordon et al, 2007), and can obscure attempts to reconstruct evolutionary history. Genes derived from syntenic regions can be paralogs (e.g.…”

Distinct and redundant expression and transcriptional diversity of MEIS gene paralogs during chicken development

“…All hits corresponded to previously identified Meis1/2 or pknox genes, confirming the absence of a Meis3 ortholog in the reference chicken genome sequence data. However, the region orthologous to the human chromosome 19q, where Meis3 is located, has been reported to be missing from the shotgun clone and bacterial artificial chromosome (BAC) libraries used in the chicken genome sequencing project, for uncertain reasons (International Chicken Genome Sequencing Consortium, 2004;Gordon et al, 2007;Dalloul et al, 2010). Therefore, it is possible that Meis3 might be absent from the reference genome assembly due to experimental reasons.…”