title: Evolution of tonoplast P-ATPase transporters involved in vacuolar acidification.
abstract: Petunia mutants (Petunia hybrida) with blue flowers defined a novel vacuolar proton pump consisting of two interacting P-ATPases, PH1 and PH5, that hyper-acidify the vacuoles of petal cells. PH5 is similar to plasma membrane H(+) P3A -ATPase, whereas PH1 is the only known eukaryoticP3B -ATPase. As there were no indications that this tonoplast pump is widespread in plants, we investigated the distribution and evolution of PH1 and PH5. We combined database mining and phylogenetic and synteny analyses of PH1- and PH5-like proteins from all kingdoms with functional analyses (mutant complementation and intracellular localization) of homologs from diverse angiosperms. We identified functional PH1 and PH5 homologs in divergent angiosperms. PH5 homologs evolved from plasma membrane P3A -ATPases, acquiring an N-terminal tonoplast-sorting sequence and new cellular function before angiosperms appeared. PH1 is widespread among seed plants and related proteins are found in some groups of bacteria and fungi and in one moss, but is absent in most algae, suggesting that its evolution involved several cases of gene loss and possibly horizontal transfer events. The distribution of PH1 and PH5 in the plant kingdom suggests that vacuolar acidification by P-ATPases appeared in gymnosperms before flowers. This implies that, next to flower color determination, vacuolar hyper-acidification is required for yet unknown processes.
authors.affiliation: Department of Plant Development and (Epi)Genetics, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098XH, Amsterdam, the Netherlands.|Department of Molecular and Cell Biology, VU-University, De Boelelaan 1081, 1071 HK, Amsterdam, the Netherlands.
authors.forename: Yanbang
authors.initials: Y
authors.lastname: Li
authors.affiliation: Department of Plant Development and (Epi)Genetics, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098XH, Amsterdam, the Netherlands.|Department of Agricultural, Forestry and Food Sciences, University of Turin, 10095, Grugliasco, Italy.
authors.forename: Sofia
authors.initials: S
authors.lastname: Provenzano
authors.affiliation: Department of Plant Development and (Epi)Genetics, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098XH, Amsterdam, the Netherlands.|Department of Molecular and Cell Biology, VU-University, De Boelelaan 1081, 1071 HK, Amsterdam, the Netherlands.
authors.forename: Mattijs
authors.initials: M
authors.lastname: Bliek
authors.affiliation: Department of Plant Development and (Epi)Genetics, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098XH, Amsterdam, the Netherlands.|Department of Molecular and Cell Biology, VU-University, De Boelelaan 1081, 1071 HK, Amsterdam, the Netherlands.
authors.forename: Cornelis
authors.initials: C
authors.lastname: Spelt
authors.affiliation: Genome Research, Faculty of Biology, Bielefeld University, 33615, Bielefeld, Germany.
authors.forename: Ingo
authors.initials: I
authors.lastname: Appelhagen
authors.affiliation: Department of Molecular and Cell Biology, VU-University, De Boelelaan 1081, 1071 HK, Amsterdam, the Netherlands.
authors.forename: Laura
authors.initials: L
authors.lastname: Machado de Faria
authors.affiliation: Department of Molecular and Cell Biology, VU-University, De Boelelaan 1081, 1071 HK, Amsterdam, the Netherlands.
authors.forename: Walter
authors.initials: W
authors.lastname: Verweij
authors.affiliation: Department of Agricultural, Forestry and Food Sciences, University of Turin, 10095, Grugliasco, Italy.
authors.forename: Andrea
authors.initials: A
authors.lastname: Schubert
authors.affiliation: Genome Research, Faculty of Biology, Bielefeld University, 33615, Bielefeld, Germany.
authors.forename: Martin
authors.initials: M
authors.lastname: Sagasser
authors.affiliation: Dynamic Cell Imaging, Faculty of Biology, Bielefeld University, 33501, Bielefeld, Germany.
authors.forename: Thorsten
authors.initials: T
authors.lastname: Seidel
authors.affiliation: Genome Research, Faculty of Biology, Bielefeld University, 33615, Bielefeld, Germany.
authors.forename: Bernd
authors.identifier: 0000-0002-7635-3473
authors.initials: B
authors.lastname: Weisshaar
authors.affiliation: Department of Plant Development and (Epi)Genetics, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098XH, Amsterdam, the Netherlands.|Department of Molecular and Cell Biology, VU-University, De Boelelaan 1081, 1071 HK, Amsterdam, the Netherlands.
authors.forename: Ronald
authors.initials: R
authors.lastname: Koes
authors.affiliation: Department of Plant Development and (Epi)Genetics, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098XH, Amsterdam, the Netherlands.|Department of Molecular and Cell Biology, VU-University, De Boelelaan 1081, 1071 HK, Amsterdam, the Netherlands.
authors.forename: Francesca
authors.initials: F
authors.lastname: Quattrocchio
mesh_terms: D000143:Acids / Q000378:metabolism*; D000595:Amino Acid Sequence; D001665:Binding Sites; D002412:Cations; D002462:Cell Membrane / Q000378:metabolism; D019143:Evolution, Molecular; D018506:Gene Expression Regulation, Plant; D026901:Membrane Transport Proteins / Q000378:metabolism*; D032306:Petunia / Q000201:enzymology*; D010802:Phylogeny; D010940:Plant Proteins / Q000737:chemistry / Q000378:metabolism; D006180:Proton-Translocating ATPases / Q000737:chemistry / Q000378:metabolism*; D027826:Rosa / Q000235:genetics; D017386:Sequence Homology, Amino Acid; D014617:Vacuoles / Q000201:enzymology* / Q000378:metabolism; D027843:Vitis / Q000235:genetics
chemical_list: D000143:Acids; D002412:Cations; D026901:Membrane Transport Proteins; D010940:Plant Proteins; D006180:Proton-Translocating ATPases
keywords: P-ATPase; phylogeny; protein evolution; proton pumps; vacuolar acidification