Abstract
Nodulin 26-like intrinsic proteins (NIPs) play essential roles in transporting the nutrients silicon and boron in seed plants, but the evolutionary origin of this transport function and the co-permeability to toxic arsenic remains enigmatic. Horizontal gene transfer of a yet uncharacterised bacterial AqpN-aquaporin group was the starting-point for plant NIP evolution. We combined intense sequence, phylogenetic and genetic context analyses and a mutational approach with various transport assays in oocytes and plants to resolve the transorganismal and functional evolution of bacterial and algal and terrestrial plant NIPs and to reveal their molecular transport specificity features. We discovered that aqpN genes are prevalently located in arsenic resistance operons of various prokaryotic phyla. We provided genetic and functional evidence that these proteins contribute to the arsenic detoxification machinery. We identified NIPs with the ancestral bacterial AqpN selectivity filter composition in algae, liverworts, moss, hornworts and ferns and demonstrated that these archetype plant NIPs and their prokaryotic progenitors are almost impermeable to water and silicon but transport arsenic and boron. With a mutational approach, we demonstrated that during evolution, ancestral NIP selectivity shifted to allow subfunctionalisations. Together, our data provided evidence that evolution converted bacterial arsenic efflux channels into essential seed plant nutrient transporters.
Highlights
The metalloids boron (B) and silicon (Si) are fundamental for the development of vascular plants because they ensure proper differentiation, structural support and elasticity of plant cell walls, and because they contribute to pathogen defence and general stress tolerance (Ma et al, 2006; Bienert & Chaumont, 2011)
Our phylogenetic analyses using 366 bacterial, archaeal and plant Nodulin 26-like intrinsic proteins (NIPs)-type major intrinsic protein (MIP) showed that the major prokaryotic MIP groups, which are AQPZs, AQPMs, AQPNs and GLPFs, formed well supported clades (Fig. 1)
Six major AQPN clades (I–VI) with a full node support were detected. Two of these AQPN clades do not encode F–A–A–R-type selectivity filter (SF) but display a wide variety of SF residue combinations: AQPN-I is mainly composed of archaeal and AQPN-II of bacterial sequences (Fig. 1)
Summary
The metalloids boron (B) and silicon (Si) are fundamental for the development of vascular plants because they ensure proper differentiation, structural support and elasticity of plant cell walls, and because they contribute to pathogen defence and general stress tolerance (Ma et al, 2006; Bienert & Chaumont, 2011). Nodulin 26-like intrinsic proteins (NIPs) mediate B and Si transport and thereby sustain growth, fertility and yield of terrestrial plants. NIPs belong to the major intrinsic protein (MIP) superfamily ( termed as aquaporins, AQPs), which comprises channels for the diffusion of small neutral and mostly polar molecules across various biological membranes in all kingdoms of life. MIP channels possess six transmembrane helices connected by five loops and the two termini facing the cytoplasm. The so-called aromatic/arginine (ar/R) constriction region acts as an MIP selectivity filter (SF) and comprises four amino acids of transmembrane helices 2 and 5 (positions R1 and R2) and loop E (positions R3 and R4) representing the narrowest part of the channel pore and forming a size exclusion barrier conferring selectivity to particular substrates (Murata et al, 2000)
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