A Phylogenetic Framework for the Aquaporin Family in Eukaryotes

Abstract

A comprehensive evolutionary analysis of aquaporins, a family of intrinsic membrane proteins that function as water channels, was conducted to establish groups of homology (i.e., to identify orthologues and paralogues) within the family and to gain insights into the functional constraints acting on the structure of the aquaporin molecule structure. Aquaporins are present in all living organisms, and therefore, they provide an excellent opportunity to further our understanding of the broader biological significance of molecular evolution by gene duplication followed by functional and structural specialization. Based on the resulting phylogeny, the 153 channel proteins analyzed were classified into six major paralogous groups: (1) GLPs, or glycerol-transporting channel proteins, which include mammalian AQP3, AQP7, and AQP9, several nematode paralogues, a yeast paralogue, and Escherichia coli GLP; (2) AQPs, or aquaporins, which include metazoan AQP0, AQP1, AQP2, AQP4, AQP5, and AQP6; (3) PIPs, or plasma membrane intrinsic proteins of plants, which include PIP1 and PIP2; (4) TIPs, or tonoplast intrinsic proteins of plants, which include alphaTIP, gammaTIP, and deltaTIP; (5) NODs, or nodulins of plants; and (6) AQP8s, or metazoan aquaporin 8 proteins. Of these groups, AQPs, PIPs, and TIPs cluster together. According to the results, the capacity to transport glycerol shown by several members of the family was acquired only early in the history of the family. The new phylogeny reveals that several water channel proteins are misclassified and require reassignment, whereas several previously undetermined ones can now be classified with confidence. The deduced phylogenetic framework was used to characterize the molecular features of water channel proteins. Three motifs are common to all family members: AEF (Ala-Glu-Phe), which is located in the N-terminal domain; and two NPA (Asp-Pro-Ala) boxes, which are located in the center and C-terminal domains, respectively. Other residues are found to be conserved within the major groups but not among them. Overall, the PIP subfamily showed the least variation. In general, no radical amino acid replacements affecting tertiary structure were identified, with the exception of Ala-->Ser in the TIP subfamily. Constancy of rates of evolution was demonstrated within the different paralogues but rejected among several of them (GLP and NOD).

Conserved elements within first intron of aquaporin-5 (Aqp5) function as transcriptional enhancers

“…In the Aqp2 gene, the conserved intronic sequence is located in intron 1, while in Aqp6 it is located in intron 3. Furthermore, evolutionary analysis of aquaporins has shown that these genes have evolved by several rounds of gene duplication [25]. The most recent gene duplication gave rise to Aqp2 and Aqp5, and it is interesting that both these genes show evolutionary conservation of the 3′ portion of intron 1.…”

Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family

“…The structures of aquaporins have been intensively studied, revealing the functions of their conserved motifs and post-translational modification sites, in water transport [3][4][5][6][7][8][9][10][11][12][13][14][15]. The expression patterns of aquaporin genes in response to salt, drought, cold, submergence, light, and phytohormones have also been characterized in various plants [16][17][18][19][20][21][22][23][24].…”

Water Transport by Aquaporins in the Extant Plant Physcomitrella patens

“…Many aquaporins (AQPs) have been detected in animal cells (Agre et al, 2001;Zardoya and Villalba, 2001;Agre and Kozono, 2003) and plant cells (Chrispeels et al, 2001;Maurel et al, 2002;Luu and Maurel, 2005;Hachez et al, 2006). Although several studies reported that AQPs may increase membrane permeability to glycerol (Stroud et al, 2003), urea (Echevarria et al, 1994), and perhaps CO 2 (Uehlein et al, 2003) or even ions (Yasui et al, 1999;Hazama et al, 2002), it is now well established that most of these transmembrane proteins increase the water permeability of cellular membranes.…”