title: Evolutionary Divergence of Plant Borate Exporters and Critical Amino Acid Residues for the Polar Localization and Boron-Dependent Vacuolar Sorting of AtBOR1.
abstract: Boron (B) is an essential micronutrient for plants but is toxic when accumulated in excess. The plant BOR family encodes plasma membrane-localized borate exporters (BORs) that control translocation and homeostasis of B under a wide range of conditions. In this study, we examined the evolutionary divergence of BORs among terrestrial plants and showed that the lycophyte Selaginella moellendorffii and angiosperms have evolved two types of BOR (clades I and II). Clade I includes AtBOR1 and homologs previously shown to be involved in efficient transport of B under conditions of limited B availability. AtBOR1 shows polar localization in the plasma membrane and high-B-induced vacuolar sorting, important features for efficient B transport under low-B conditions, and rapid down-regulation to avoid B toxicity. Clade II includes AtBOR4 and barley Bot1 involved in B exclusion for high-B tolerance. We showed, using yeast complementation and B transport assays, that three genes in S. moellendorffii, SmBOR1 in clade I and SmBOR3 and SmBOR4 in clade II, encode functional BORs. Furthermore, amino acid sequence alignments identified an acidic di-leucine motif unique in clade I BORs. Mutational analysis of AtBOR1 revealed that the acidic di-leucine motif is required for the polarity and high-B-induced vacuolar sorting of AtBOR1. Our data clearly indicated that the common ancestor of vascular plants had already acquired two types of BOR for low- and high-B tolerance, and that the BOR family evolved to establish B tolerance in each lineage by adapting to their environments.
authors.affiliation: Graduate School of Agriculture, Hokkaido University, Sapporo, 060-8589 Japan.
authors.forename: Shinji
authors.initials: S
authors.lastname: Wakuta
authors.affiliation: Computational Bioscience Research Center, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia.
authors.forename: Katsuhiko
authors.initials: K
authors.lastname: Mineta
authors.affiliation: Graduate School of Agriculture, Hokkaido University, Sapporo, 060-8589 Japan.
authors.forename: Taro
authors.initials: T
authors.lastname: Amano
authors.affiliation: Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, 113-8657 Japan.
authors.forename: Atsushi
authors.initials: A
authors.lastname: Toyoda
authors.affiliation: Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, 113-8657 Japan.
authors.forename: Toru
authors.initials: T
authors.lastname: Fujiwara
authors.affiliation: Graduate School of Agriculture, Hokkaido University, Sapporo, 060-8589 Japan Graduate School of Life Science, Hokkaido University, Sapporo, 060-8589 Japan.
authors.forename: Satoshi
authors.initials: S
authors.lastname: Naito
authors.affiliation: Graduate School of Agriculture, Hokkaido University, Sapporo, 060-8589 Japan jtakano@abs.agr.hokudai.ac.jp.
authors.forename: Junpei
authors.initials: J
authors.lastname: Takano
mesh_terms: D020816:Amino Acid Motifs; D000595:Amino Acid Sequence; D000596:Amino Acids / Q000378:metabolism*; D017920:Antiporters / Q000378:metabolism*; D017360:Arabidopsis / Q000187:drug effects / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000378:metabolism*; D001692:Biological Transport; D001881:Borates / Q000378:metabolism*; D001895:Boron / Q000378:metabolism*; D019068:Bryopsida / Q000378:metabolism; D016764:Cell Polarity; D003001:Cloning, Molecular; D017124:Conserved Sequence; D018076:DNA, Complementary / Q000235:genetics; D019143:Evolution, Molecular; D008969:Molecular Sequence Data; D009154:Mutation / Q000235:genetics; D010802:Phylogeny; D032503:Selaginellaceae / Q000378:metabolism; D016415:Sequence Alignment; D014617:Vacuoles / Q000378:metabolism*
chemical_list: D000596:Amino Acids; D017920:Antiporters; D029681:Arabidopsis Proteins; C469216:BOR1 protein, Arabidopsis; D001881:Borates; D018076:DNA, Complementary; D001895:Boron
keywords: Boron; Evolution; Exporter; Membrane trafficking