Dynamic evolution of transient receptor potential vanilloid (TRPV) ion channel family with numerous gene duplications and losses
Marina Morini, Christina A. Bergqvist, Juan F. Asturiano, Dan Larhammar, Sylvie Dufour
Abstract
The transient
receptor potential vanilloid (TRPV) ion channel family is involved in multiple
sensory and physiological functions including thermosensing and
temperature-dependent neuroendocrine regulation. The objective of the present
study was to investigate the number, origin and evolution of TRPV genes in
metazoans, with special focus on the impact of the vertebrate whole-genome
duplications (WGD). Gene searches followed by phylogenetic and synteny analyses
revealed multiple previously undescribed TRPV genes. The common ancestor of
Cnidaria and Bilateria had three TRPV genes that became four in the
deuterostome ancestor. Two of these were lost in the vertebrate ancestor. The
remaining two genes gave rise to two TRPV subfamilies in vertebrates,
consisting of subtypes 1, 2, 3, 4, 9 and 5, 6, 7, 8, respectively. This gene
expansion resulted from the two basal vertebrate WGD events (1R and 2R) and
three local duplications before the radiation of gnathostomes. TRPV1, 4 and 5
have been retained in all gnathostomes investigated, presumably reflecting
important functions. TRPV7 and 8 have been lost independently in various
lineages but are still retained in cyclostomes, actinistians (coelacanth),
amphibians, prototherians and basal actinopterygians (Polypteridae). TRPV3 and
9 are present in extant elasmobranchs, while TRPV9 was lost in the osteichthyan
ancestor and TRPV3 in the actinopterygian ancestor. The coelacanth has retained
the ancestral osteichthyan repertoire of TRPV1, 3, 4, 5, 7 and 8. TRPV2 arose
in the tetrapod ancestor. Duplications of TRPV5 occurred independently in
various lineages, such as cyclostomes, chondrichthyans, anuran amphibians,
sauropsids, mammals (where the duplicate is called TRPV6), and actinopterygians
(Polypteridae and Esocidae). After the teleost-specific WGD (3R) only TRPV1
retained its duplicate, whereas TRPV4 and 5 remained as single genes. Both
3R-paralogs of TRPV1 were kept in some teleost species, while one paralog was
lost in others. The salmonid-specific WGD (4R) duplicated TRPV1, 4, and 5
leading to six TRPV genes. The largest number was found in Xenopus tropicalis
with no less than 15 TRPV genes. This study provides a comprehensive
evolutionary scenario for the vertebrate TRPV family, revealing additional TRPV
types and proposing a phylogeny-based classification of TRPV across metazoans.
Frontiers in Endocrinology 13:1013868 (23 pp) (2022)
