Abstract
BackgroundVertebrate Emx genes, retained as multiple copies, are expressed in a nested pattern in the early embryonic forebrain and required for its regionalization. This pattern seems to have originated in a vertebrate common ancestor; however, a previous analysis, reporting two lamprey Emx genes, claimed independent Emx gene duplications in both cyclostome (extant jawless fish) and gnathostome (jawed vertebrate) lineages after their divergence. This scenario is neither parsimonious nor consistent with the hypothesis that genome expansion occurred before the cyclostome-gnathostome split, which is supported by recent genome-wide analyses.ResultsWe isolated and sequenced cDNA of two hagfish Emx genes and performed intensive molecular phylogenetic analyses, including the hagfish and/or lamprey Emx genes. The lamprey genes tended to attract each other in inferred phylogenetic trees, an effect that tended to be relaxed on inclusion of the hagfish genes. The results of these analyses suggest that cyclostome EmxB is orthologous to gnathostome Emx2, which was also supported by conserved synteny. Homopolymeric amino acid (HPAA) tracts represent a remarkable feature of the lamprey Emx sequences, and a comparative genome-wide scan revealed that lamprey proteins exhibit a unique pattern of HPAA tract accumulation.ConclusionsOur analysis, including hagfish Emx genes, suggests that gene duplications gave rise to Emx1, -2 and -3 before the cyclostome-gnathostome split. We propose that independent HPAA tract accumulations in multiple ancient duplicates, as identified in lamprey Emx gene products, may have led to erroneous identification of gene duplication in the lamprey lineage. Overall, our reanalysis favors the scenario that the nested Emx expression pattern in mouse and lamprey shares a common origin.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0351-z) contains supplementary material, which is available to authorized users.
Highlights
Vertebrate Emx genes, retained as multiple copies, are expressed in a nested pattern in the early embryonic forebrain and required for its regionalization
In the early embryonic forebrain, Emx2 is expressed widely in the pallium, which develops into the cerebral cortex, while the expression of Emx1 is observed in the dorsal, medial and lateral pallium, but not the ventral pallium which later differentiates to form a part of the claustroamygdaloid complex in mammals [4]
Emx gene repertoire in diverse vertebrates including cyclostomes To make a comprehensive comparison of vertebrate Emx genes, we collected a wide range of vertebrate Emx sequences, including cyclostomes
Summary
Vertebrate Emx genes, retained as multiple copies, are expressed in a nested pattern in the early embryonic forebrain and required for its regionalization This pattern seems to have originated in a vertebrate common ancestor; a previous analysis, reporting two lamprey Emx genes, claimed independent Emx gene duplications in both cyclostome (extant jawless fish) and gnathostome (jawed vertebrate) lineages after their divergence. This scenario is neither parsimonious nor consistent with the hypothesis that genome expansion occurred before the cyclostome-gnathostome split, which is supported by recent genome-wide analyses. Assigning orthology of jawless fish genes to gnathostome counterparts is often not straightforward [14], possibly due to the high GC content and biased amino acid composition of lamprey genes [12,15,16]
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