Genome-Wide Identification, Structure Characterization, and Expression Pattern Profiling of the Aquaporin Gene Family in Betula pendula

Abstract

Aquaporin water channels (AQPs) constitute a large family of transmembrane proteins present throughout all kingdoms of life. They play key roles in the flux of water and many solutes across the membranes. The AQP diversity, protein features, and biological functions of silver birch are still unknown. A genome analysis of Betula pendula identified 33 putative genes encoding full-length AQP sequences (BpeAQPs). They are grouped into five subfamilies, representing ten plasma membrane intrinsic proteins (PIPs), eight tonoplast intrinsic proteins (TIPs), eight NOD26-like intrinsic proteins (NIPs), four X intrinsic proteins (XIPs), and three small basic intrinsic proteins (SIPs). The BpeAQP gene structure is conserved within each subfamily, with exon numbers ranging from one to five. The predictions of the aromatic/arginine selectivity filter (ar/R), Froger’s positions, specificity-determining positions, and 2D and 3D biochemical properties indicate noticeable transport specificities to various non-aqueous substrates between members and/or subfamilies. Nevertheless, overall, the BpePIPs display mostly hydrophilic ar/R selective filter and lining-pore residues, whereas the BpeTIP, BpeNIP, BpeSIP, and BpeXIP subfamilies mostly contain hydrophobic permeation signatures. Transcriptional expression analyses indicate that 23 BpeAQP genes are transcribed, including five organ-related expressions. Surprisingly, no significant transcriptional expression is monitored in leaves in response to cold stress (6 °C), although interesting trends can be distinguished and will be discussed, notably in relation to the plasticity of this pioneer species, B. pendula. The current study presents the first detailed genome-wide analysis of the AQP gene family in a Betulaceae species, and our results lay a foundation for a better understanding of the specific functions of the BpeAQP genes in the responses of the silver birch trees to cold stress.

Genome-wide identification of Fagus sylvatica aquaporins and their comparative spring and summer expression profiles

“…With an average of 2 each, FsSIPs and FsXIPs had the lowest numbers of introns and exons. This genetic structure is very similar to that found among aquaporins in other plant species (Chaumont et al 2001;Johanson et al 2001;Sakurai et al 2005;Gupta and Sankararamakrishnan 2009;Park et al 2010;Zou et al 2015b;Liu et al 2019;Wei et al 2019;Venisse et al 2021). Furthermore, conserved gene motifs as identified in MEME, are also shown in Fig.…”

“…We identified 45 non-redundant aquaporin isoforms in the F. sylvatica genome, which, in light of the 33 isoforms discovered in silver birch (Betula pendula) and the 55 isoforms in poplar (Populus trichocarpa), is well within the expected range (Gupta and Sankararamakrishnan 2009;Venisse et al 2021). Likewise, the distribution of the identified isoforms across the five subfamilies and their overall genomic structure in terms of the exon-intron arrangement is as we would expect, when compared to other woody species (Wei et al 2019;Jiang et al 2020;Venisse et al 2021).…”

“…None of the FsSIPs were predicted to have any non-water substrate permeability, which is consistent with the lack of existing reports of such permeability (Zou et al 2015a), and in light of their localisation to the endoplasmic reticulum (Ishikawa et al 2005) perhaps not surprising. However, the ar/R constriction of FsSIPs and SIPs in general is variable, which would suggest SIPs to be permeable to substrates other than water (Venisse et al 2021). Interestingly, FsXIPs also had remarkably few potential non-water substrates, which is surprising, because XIPs have been reported to conduct urea and boric acid (Wei et al 2019) as well as glycerol and H 2 O 2 (Deshmukh et al 2013).…”

“…and cotton (Gossypium sp. ), while purging events resulted in the loss of XIPs in others, such as the monocots (Gupta and Sankararamakrishnan 2009;Sonah et al 2017;Jiang et al 2020;Venisse et al 2021). In addition, aquaporins, like any other gene, are subject to natural selection pressures, resulting in differences in their numbers across species as well as differences in their relative abundance across the five subfamilies (Table 1).…”

Leaf and Branch Hydraulic Plasticity of Two Light-Demanding Broadleaved Tree Species Differing in Water-Use Strategy

“…The light-induced rapid enhancement of K L has been shown to originate from the outside-xylem compartment of the leaf [34,57] being specifically related to the up-regulation of aquaporins (AQPs) through enhanced gene expression and/or post-translational protein activation in response to irradiance. In B. pendula, a genome analysis has identified 33 putative genes encoding full-length AQP sequences [59]. The light-dependent increase of K L shows a tight correlation with AQP gene transcript abundance [60][61][62][63][64].…”