Evolution and differential expression of a vertebrate vitellogenin gene cluster
Roderick Nigel Finn
2
Jelena Kolarevic
1
2
Heidi Kongshaug
0
Frank Nilsen
0
2
0
Institute of Marine Research
,
Post box 1870 Nordnes, N-5817 Bergen
,
Norway
1
Nofima Marine
,
N-6600 Sunndalsra
,
Norway
2
Department of Biology, University of Bergen, Bergen High Technology Center
,
Postbox 7803, N-5020, Bergen
,
Norway
Background: The multiplicity or loss of the vitellogenin (vtg) gene family in vertebrates has been argued to have broad implications for the mode of reproduction (placental or non-placental), cleavage pattern (meroblastic or holoblastic) and character of the egg (pelagic or benthic). Earlier proposals for the existence of three forms of vertebrate vtgs present conflicting models for their origin and subsequent duplication. Results: By integrating phylogenetics of novel vtg transcripts from old and modern teleosts with syntenic analyses of all available genomic variants of non-metatherian vertebrates we identify the gene orthologies between the Sarcopterygii (tetrapod branch) and Actinopterygii (fish branch). We argue that the vertebrate vtg gene cluster originated in proto-chromosome m, but that vtg genes have subsequently duplicated and rearranged following whole genome duplications. Sequencing of a novel fourth vtg transcript in labrid species, and the presence of duplicated paralogs in certain model organisms supports the notion that lineage-specific gene duplications frequently occur in teleosts. The data show that the vtg gene cluster is more conserved between acanthomorph teleosts and tetrapods, than in ostariophysan teleosts such as the zebrafish. The differential expression of the labrid vtg genes are further consistent with the notion that neofunctionalized Aatype vtgs are important determinants of the pelagic or benthic character of the eggs in acanthomorph teleosts. Conclusion: The vertebrate vtg gene cluster existed prior to the separation of Sarcopterygii from Actinopterygii >450 million years ago, a period associated with the second round of whole genome duplication. The presence of higher copy numbers in a more highly expressed subcluster is particularly prevalent in teleosts. The differential expression and latent neofunctionalization of vtg genes in acanthomorph teleosts is an adaptive feature associated with oocyte hydration and spawning in the marine environment.
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Background
A defining feature of the early development of
non-eutherian vertebrates is a cleidoic egg endowed with variable
amounts of yolk. Until very recently, the major products
of the vitellogenin (vtg) genes that encode yolk proteins
have been considered to be simple precursors of the
energy reserve of vertebrate eggs, but the latest studies
have demonstrated several non-nutritional roles for Vtg
[1,2]. Similarly, the recent observation that remnants of
vtg genes exist in Eutheria, including humans, but have
sequentially been lost through co-evolution with casein
genes [3] elegantly demonstrated that the three known vtg
genes in birds represent a conserved gene complement. In
a previous study, Finn & Kristoffersen [4] proposed a
model for the evolution and neofunctionalization of vtg
genes in acanthomorph teleosts. We identified vtgC as an
ancestral gene, and argued that the dual vtgAa/vtgAb
system, first noted by La Fleur et al. [5] was derived from a
single form, the A-type vtg. In this model, the separation
of the vtgC- and vtgA-type genes occurred following the
second round (R2) of whole genome duplication (WGD).
Subsequently vtgA duplicated and formed paragolous
vtgAa and vtgAb genes in acanthomorph teleosts. This
phylogenetic model has been corroborated by other
investigators [6]. Most recently however, Babin [7] has provided a
syntenic map of vertebrate vtg genes, which shows that the
three forms of vtg are encoded in a vtg gene cluster (VGC)
in non-eutherian vertebrates. A major goal of the present
study was to integrate the statistical, biochemical and
physical models of vtg gene evolution in vertebrates.
Through a series of studies, we and other laboratories have
shown that the pelagic nature of a marine teleost egg is an
evolved feature [4] that primarily results from the
maturational influx of water due to differential degradation of
VtgAa-type yolk proteins (Yp), and the temporal insertion
of novel aquaporins (Aqp1b) in the microvillous portion
of the plasmalemma [8-10]. The neofunctionalization of
the vtgAa form in acanthomorph teleosts, has sensitized
the heavy chain domain (LvH-Aa) to catheptic proteolysis
that generates a large organic osmolyte pool of free amino
acids (FAA) in the ovulated egg [1,9,11-19]. In contrast
the LvH domains derived from vtgAb and vtgC genes may
be partially cleaved, but remain mostly intact following
the maturational proteolytic event, and thus contribute
minimally to oocyte hydration [1,12,14,17,18]. In
teleosts that spawn benthic eggs (benthophils), a character
that we have argued to be the ancestral condition due to
an ancient freshwater heritage (Finn & (...truncated)