Evolutionary divergence of plant borate exporters and critical amino acid residues for the polar localization and boron-dependent vacuolar sorting of AtBOR1

Handle URI:
http://hdl.handle.net/10754/564020
Title:
Evolutionary divergence of plant borate exporters and critical amino acid residues for the polar localization and boron-dependent vacuolar sorting of AtBOR1
Authors:
Wakuta, Shinji; Mineta, Katsuhiko ( 0000-0002-4727-045X ) ; Amano, Taro; Toyoda, Atsushi; Fujiwara, Toru; Naito, Satoshi; Takano, Junpei
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. © The Author 2015. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
KAUST Department:
Computational Bioscience Research Center (CBRC)
Publisher:
Oxford University Press (OUP)
Journal:
Plant and Cell Physiology
Issue Date:
24-Jan-2015
DOI:
10.1093/pcp/pcv011
Type:
Article
ISSN:
00320781
Sponsors:
This work was supported by the the Japan Society for the Promotion of Science (JSPS) [Funding Program for Next Generation World-Leading Researchers (NEXT) program and Grants-in-Aid for Scientific Research (26712007) to J.T.]; the Human Frontier Science Program (HFSP) [Young Investigators Grant to J.T.].
Appears in Collections:
Articles; Computational Bioscience Research Center (CBRC)

Full metadata record

DC FieldValue Language
dc.contributor.authorWakuta, Shinjien
dc.contributor.authorMineta, Katsuhikoen
dc.contributor.authorAmano, Taroen
dc.contributor.authorToyoda, Atsushien
dc.contributor.authorFujiwara, Toruen
dc.contributor.authorNaito, Satoshien
dc.contributor.authorTakano, Junpeien
dc.date.accessioned2015-08-03T12:28:43Zen
dc.date.available2015-08-03T12:28:43Zen
dc.date.issued2015-01-24en
dc.identifier.issn00320781en
dc.identifier.doi10.1093/pcp/pcv011en
dc.identifier.urihttp://hdl.handle.net/10754/564020en
dc.description.abstractBoron (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. © The Author 2015. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.en
dc.description.sponsorshipThis work was supported by the the Japan Society for the Promotion of Science (JSPS) [Funding Program for Next Generation World-Leading Researchers (NEXT) program and Grants-in-Aid for Scientific Research (26712007) to J.T.]; the Human Frontier Science Program (HFSP) [Young Investigators Grant to J.T.].en
dc.publisherOxford University Press (OUP)en
dc.subjectBoronen
dc.subjectEvolutionen
dc.subjectExporteren
dc.subjectMembrane traffickingen
dc.titleEvolutionary divergence of plant borate exporters and critical amino acid residues for the polar localization and boron-dependent vacuolar sorting of AtBOR1en
dc.typeArticleen
dc.contributor.departmentComputational Bioscience Research Center (CBRC)en
dc.identifier.journalPlant and Cell Physiologyen
dc.contributor.institutionGraduate School of Agriculture, Hokkaido University, Sapporo, Japanen
dc.contributor.institutionGraduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, Japanen
dc.contributor.institutionGraduate School of Life Science, Hokkaido University, Sapporo, Japanen
kaust.authorMineta, Katsuhikoen
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