Genome duplication, subfunction partitioning, and lineage divergence:Sox9in stickleback and zebrafish

Abstract

Teleosts are the most species-rich group of vertebrates, and a genome duplication (tetraploidization) event in ray-fin fish appears to have preceded this remarkable explosion of biodiversity. What is the relationship of the ray-fin genome duplication to the teleost radiation? Genome duplication may have facilitated lineage divergence by partitioning different ancestral gene subfunctions among co-orthologs of tetrapod genes in different teleost lineages. To test this hypothesis, we investigated gene expression patterns for Sox9 gene duplicates in stickleback and zebrafish, teleosts whose lineages diverged early in Euteleost evolution. Most expression domains appear to have been partitioned between Sox9a and Sox9b before the divergence of stickleback and zebrafish lineages, but some ancestral expression domains were distributed differentially in each lineage. We conclude that some gene subfunctions, as represented by lineage-specific expression domains, may have assorted differently in separate lineages and that these may have contributed to lineage diversification during teleost evolution. Developmental Dynamics 228:480 -489, 2003.

Genome evolution and biodiversity in teleost fish

“…In this case, both copies are preserved, since the presence of both is necessary to perform the original function of the ancestral single-copy gene. In teleosts, the evolution of numerous gene duplicates is consistent with the subfunctionalization model (eg Lister et al, 2001;Serluca et al, 2001;Altschmied et al, 2002;McClintock et al, 2002;Cresko et al, 2003;Yu et al, 2003;Amores et al, 2004). For example, mammals and birds have a unique microphthalmia-associated transcription factor gene mitf, from which different isoforms are expressed through the use of different promoter sequences and alternative exons.…”

“…In the rare examples like mitfa/mitfb or sox9a/sox9b, for which gene duplicate expression and function have been examined in divergent fish species, the major partitioning of ancestral gene functions appears to be ancient (Lister et al, 2001;Altschmied et al, 2002;Cresko et al, 2003). This is manifested by paralog-specific subfunctions conserved in divergent fishes.…”

Duplication and divergence of fgf8 functions in teleost development and evolution

“…We screened our stickleback fosmid genomic library (see Cresko et al, 2003 for details) by polymerase chain reaction (PCR) using degenerate primers designed from the first exon of the zebrafish fgf8, fgf17b, fgf18, and fgf24 sequences. (Note that we use here the official gene and protein nomenclature conventions of zebrafish for stickleback; we use the mouse convention for generalized chordate genes or species without official conventions, and the human convention for human genes.…”

“…Stickleback embryos were staged relative to zebrafish embryos using the zebrafish staging series (Kimmel et al,'95). In our system, stickleback development at 201C is roughly 2.5 times slower than for zebrafish at 27.51C (Cresko et al, 2003). The University of Oregon IACUC approved experiments for this study.…”

“…In this context, nonfunctionalization, subfunction partitioning, and neofunctionalization, occurring independently in separate lineages, could lead to different functions, differential subfunction partitioning, relaxation of pleiotropic constraints, and speciation (Lynch and Force, 2000;Taylor et al, 2001;Postlethwait et al, 2004;Force et al, 2004Force et al, , 2005. Empirical studies have shown great support for the molecular mechanisms of the subfunctionalization model (Lister et al, 2001;Altschmied et al, 2002;Cresko et al, 2003;Liu et al, 2005).…”