Origins and functional diversification of salinity‐responsive Na⁺, K⁺ATPase α1 paralogs in salmonids

Abstract

The Salmoniform whole-genome duplication is hypothesized to have facilitated the evolution of anadromy, but little is known about the contribution of paralogs from this event to the physiological performance traits required for anadromy, such as salinity tolerance. Here, we determined when two candidate, salinity-responsive paralogs of the Na(+) , K(+) ATPase α subunit (α1a and α1b) evolved and studied their evolutionary trajectories and tissue-specific expression patterns. We found that these paralogs arose during a small-scale duplication event prior to the Salmoniform, but after the teleost, whole-genome duplication. The 'freshwater paralog' (α1a) is primarily expressed in the gills of Salmoniformes and an unduplicated freshwater sister species (Esox lucius) and experienced positive selection in the freshwater ancestor of Salmoniformes and Esociformes. Contrary to our predictions, the 'saltwater paralog' (α1b), which is more widely expressed than α1a, did not experience positive selection during the evolution of anadromy in the Coregoninae and Salmonine. To determine whether parallel mutations in Na(+) , K(+) ATPase α1 may contribute to salinity tolerance in other fishes, we studied independently evolved salinity-responsive Na(+) , K(+) ATPase α1 paralogs in Anabas testudineus and Oreochromis mossambicus. We found that a quarter of the mutations occurring between salmonid α1a and α1b in functionally important sites also evolved in parallel in at least one of these species. Together, these data argue that paralogs contributing to salinity tolerance evolved prior to the Salmoniform whole-genome duplication and that strong selection and/or functional constraints have led to parallel evolution in salinity-responsive Na(+) , K(+) ATPase α1 paralogs in fishes.

Transcriptomic imprints of adaptation to fresh water: parallel evolution of osmoregulatory gene expression in the Alewife

“…Two of the ion‐uptake transcripts of the atp1a1 gene (transcripts 7 and 8) were homologous to the ‘FW’ isoform of NKA α1 (NKA α 1a) in other fishes (Dalziel et al . ) and were named accordingly (NKA α1a transcripts 7 and 8; Table ). FW expression of NKA α1a transcript 7 was sevenfold higher in both landlocked populations compared to A‐Bride (Fig.…”

“…One of these transcripts was analogous to NKA α1b, the ‘SW’ isoform of atp1a1 , and was named as such (Dalziel et al . ; NKA α1b transcript 9; Table ). In SW, expression of this transcript was significantly lower in both landlocked populations (Fig.…”

“…; Dalziel et al . ). Our results add to this growing body of literature suggesting that salinity‐dependent paralogs have evolved in multiple, unrelated lineages.…”

Reduced salinity tolerance in the Arctic grayling (Thymallus arcticus) is associated with rapid development of a gill interlamellar cell mass: implications of high-saline spills on native freshwater salmonids

“…Sodium–potassium ATPase (NKA) plays an important role in maintaining systemic and cellular ionic homeostasis, and its various isoforms have been identified to have a strong influence on the ability to tolerate seawater [ nkaα1a as the freshwater isoform and nkaα1b as the seawater isoform ( Richards et al ., 2003 ; Bystriansky et al ., 2006 ; Nilsen et al ., 2007 ; Bystriansky and Schulte, 2011 )]. Indeed, a recent phylogenetic analysis of the Salmonidae family has identified nkaα1a and nkaα1b sequences in all three subfamilies: Salmoninae, Coregoninae and Thymallinae (salmon and trout, whitefish and grayling, respectively; Dalziel et al ., 2014 ).…”

Assessment of the timing and degree of smolt development in southern populations of masu salmon Oncorhynchus masou

“…NKA is composed of two essential subunits, α and β and one regulatory subunit, γ (Blanco & Mercer, 1998;Geering, 2006Geering, , 2008Mobasheri et al, 2000). Multiple isoforms of NKA α and β subunits have been found in vertebrates (Blanco & Mercer, 1998;Geering, 2008) and teleosts possess additional isoforms due to an extra round of whole genome duplication (Dalziel et al, 2014;Rajarao et al, 2001;Serluca et al, 2001). There are five isoforms of NKA α subunits in salmonids, of which an isoform named α1b is considered as seawater type while α1a is a freshwater type based on their responses to salinity increases (Bystriansky et al, 2006;Madsen et al, 2009;McCormick et al, 2009;Richards et al, 2003).…”