Expansion of voltage-dependent Na+ channel gene family in early tetrapods coincided with the emergence of terrestriality and increased brain complexity
Expansion of voltage-dependent Na+ channel gene family in early tetrapods coincided with the emergence of terrestriality and increased brain complexity
Date
2010-11-29
Authors
Zakon, Harold H.
Jost, Manda C.
Lu, Ying
Jost, Manda C.
Lu, Ying
Linked Authors
Alternative Title
Citable URI
As Published
Date Created
Location
DOI
Related Materials
Replaces
Replaced By
Keywords
Sodium channel
Tetrapods
Amniotes
Terrestriality
Gene duplication
Brain
Tetrapods
Amniotes
Terrestriality
Gene duplication
Brain
Abstract
Mammals have 10 voltage-dependent sodium (Nav) channel genes. Nav
channels are expressed in different cell types with different sub-cellular
distributions and are critical for many aspects of neuronal processing. The last
common ancestor of teleosts and tetrapods had four Nav channel genes
presumably on four different chromosomes. In the lineage leading to mammals a
series of tandem duplications on two of these chromosomes more than doubled
the number of Nav channel genes. It is unknown when these duplications
occurred, whether they occurred against a backdrop of duplication of flanking
genes on their chromosomes, or as an expansion of ion channel genes in
general. We estimated key dates of the Nav channel gene family expansion by
phylogenetic analysis using teleost, elasmobranch, lungfish, amphibian, avian,
lizard, and mammalian Nav channel sequences, as well as chromosomal synteny
for tetrapod genes. We tested, and exclude, the null hypothesis that Nav
channel genes reside in regions of chromosomes prone to duplication by
demonstrating the lack of duplication or duplicate retention of surrounding genes.
We also find no comparable expansion in other voltage dependent ion channel
gene families of tetrapods following the teleost-tetrapod divergence. We posit a
specific expansion of the Nav channel gene family in the Devonian and
Carboniferous periods when tetrapods evolved, diversified, and invaded the
terrestrial habitat. During this time the amniote forebrain evolved greater
anatomical complexity and novel tactile sensory receptors appeared. The
duplication of Nav channel genes allowed for greater regional specialization in
Nav channel expression, variation in sub-cellular localization, and enhanced
processing of somatosensory input.
Description
Author Posting. © The Authors, 2010. This is the author's version of the work. It is posted here by permission of Oxford University Press for personal use, not for redistribution. The definitive version was published in Molecular Biology and Evolution 28 (2011): 1415-1424, doi:10.1093/molbev/msq325.