title: Envelope K+/H+ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development.
abstract: It is well established that thylakoid membranes of chloroplasts convert light energy into chemical energy, yet the development of chloroplast and thylakoid membranes is poorly understood. Loss of function of the two envelope K(+)/H(+) antiporters AtKEA1 and AtKEA2 was shown previously to have negative effects on the efficiency of photosynthesis and plant growth; however, the molecular basis remained unclear. Here, we tested whether the previously described phenotypes of double mutant kea1kea2 plants are due in part to defects during early chloroplast development in Arabidopsis (Arabidopsis thaliana). We show that impaired growth and pigmentation is particularly evident in young expanding leaves of kea1kea2 mutants. In proliferating leaf zones, chloroplasts contain much lower amounts of photosynthetic complexes and chlorophyll. Strikingly, AtKEA1 and AtKEA2 proteins accumulate to high amounts in small and dividing plastids, where they are specifically localized to the two caps of the organelle separated by the fission plane. The unusually long amino-terminal domain of 550 residues that precedes the antiport domain appears to tether the full-length AtKEA2 protein to the two caps. Finally, we show that the double mutant contains 30% fewer chloroplasts per cell. Together, these results show that AtKEA1 and AtKEA2 transporters in specific microdomains of the inner envelope link local osmotic, ionic, and pH homeostasis to plastid division and thylakoid membrane formation.
authors.affiliation: Departimento de Bioquímica, Biología Celular, y Molecular de Plantas, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, 18008 Granada, Spain (M.N.A.-S., A.A., O.C., M.P.R.-R., K.V.);Howard Hughes Medical Institute, Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (U.A.);Institute of Plant Biochemistry, Heinrich-Heine-University Düsseldorf, D-40225 Duesseldorf, Germany (T.S., P.J.);School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236 (H.-H.K.); andDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742 (H.S.).
authors.forename: María Nieves
authors.initials: MN
authors.lastname: Aranda-Sicilia
authors.affiliation: Departimento de Bioquímica, Biología Celular, y Molecular de Plantas, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, 18008 Granada, Spain (M.N.A.-S., A.A., O.C., M.P.R.-R., K.V.);Howard Hughes Medical Institute, Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (U.A.);Institute of Plant Biochemistry, Heinrich-Heine-University Düsseldorf, D-40225 Duesseldorf, Germany (T.S., P.J.);School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236 (H.-H.K.); andDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742 (H.S.).
authors.forename: Ali
authors.identifier: 0000-0002-0395-9669
authors.initials: A
authors.lastname: Aboukila
authors.affiliation: Departimento de Bioquímica, Biología Celular, y Molecular de Plantas, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, 18008 Granada, Spain (M.N.A.-S., A.A., O.C., M.P.R.-R., K.V.);Howard Hughes Medical Institute, Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (U.A.);Institute of Plant Biochemistry, Heinrich-Heine-University Düsseldorf, D-40225 Duesseldorf, Germany (T.S., P.J.);School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236 (H.-H.K.); andDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742 (H.S.).
authors.forename: Ute
authors.initials: U
authors.lastname: Armbruster
authors.affiliation: Departimento de Bioquímica, Biología Celular, y Molecular de Plantas, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, 18008 Granada, Spain (M.N.A.-S., A.A., O.C., M.P.R.-R., K.V.);Howard Hughes Medical Institute, Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (U.A.);Institute of Plant Biochemistry, Heinrich-Heine-University Düsseldorf, D-40225 Duesseldorf, Germany (T.S., P.J.);School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236 (H.-H.K.); andDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742 (H.S.).
authors.forename: Olivier
authors.identifier: 0000-0003-2751-969X
authors.initials: O
authors.lastname: Cagnac
authors.affiliation: Departimento de Bioquímica, Biología Celular, y Molecular de Plantas, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, 18008 Granada, Spain (M.N.A.-S., A.A., O.C., M.P.R.-R., K.V.);Howard Hughes Medical Institute, Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (U.A.);Institute of Plant Biochemistry, Heinrich-Heine-University Düsseldorf, D-40225 Duesseldorf, Germany (T.S., P.J.);School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236 (H.-H.K.); andDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742 (H.S.).
authors.forename: Tobias
authors.initials: T
authors.lastname: Schumann
authors.affiliation: Departimento de Bioquímica, Biología Celular, y Molecular de Plantas, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, 18008 Granada, Spain (M.N.A.-S., A.A., O.C., M.P.R.-R., K.V.);Howard Hughes Medical Institute, Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (U.A.);Institute of Plant Biochemistry, Heinrich-Heine-University Düsseldorf, D-40225 Duesseldorf, Germany (T.S., P.J.);School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236 (H.-H.K.); andDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742 (H.S.).
authors.forename: Hans-Henning
authors.identifier: 0000-0001-8000-0817
authors.initials: HH
authors.lastname: Kunz
authors.affiliation: Departimento de Bioquímica, Biología Celular, y Molecular de Plantas, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, 18008 Granada, Spain (M.N.A.-S., A.A., O.C., M.P.R.-R., K.V.);Howard Hughes Medical Institute, Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (U.A.);Institute of Plant Biochemistry, Heinrich-Heine-University Düsseldorf, D-40225 Duesseldorf, Germany (T.S., P.J.);School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236 (H.-H.K.); andDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742 (H.S.).
authors.forename: Peter
authors.identifier: 0000-0002-5340-1153
authors.initials: P
authors.lastname: Jahns
authors.affiliation: Departimento de Bioquímica, Biología Celular, y Molecular de Plantas, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, 18008 Granada, Spain (M.N.A.-S., A.A., O.C., M.P.R.-R., K.V.);Howard Hughes Medical Institute, Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (U.A.);Institute of Plant Biochemistry, Heinrich-Heine-University Düsseldorf, D-40225 Duesseldorf, Germany (T.S., P.J.);School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236 (H.-H.K.); andDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742 (H.S.).
authors.forename: María Pilar
authors.identifier: 0000-0001-7711-3239
authors.initials: MP
authors.lastname: Rodríguez-Rosales
authors.affiliation: Departimento de Bioquímica, Biología Celular, y Molecular de Plantas, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, 18008 Granada, Spain (M.N.A.-S., A.A., O.C., M.P.R.-R., K.V.);Howard Hughes Medical Institute, Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (U.A.);Institute of Plant Biochemistry, Heinrich-Heine-University Düsseldorf, D-40225 Duesseldorf, Germany (T.S., P.J.);School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236 (H.-H.K.); andDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742 (H.S.).
authors.forename: Heven
authors.identifier: 0000-0003-4118-3758
authors.initials: H
authors.lastname: Sze
authors.affiliation: Departimento de Bioquímica, Biología Celular, y Molecular de Plantas, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, 18008 Granada, Spain (M.N.A.-S., A.A., O.C., M.P.R.-R., K.V.);Howard Hughes Medical Institute, Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (U.A.);Institute of Plant Biochemistry, Heinrich-Heine-University Düsseldorf, D-40225 Duesseldorf, Germany (T.S., P.J.);School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236 (H.-H.K.); andDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742 (H.S.) kev@eez.csic.es.
authors.forename: Kees
authors.identifier: 0000-0001-5177-6464
authors.initials: K
authors.lastname: Venema
mesh_terms: D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D002734:Chlorophyll / Q000378:metabolism; D002736:Chloroplasts / Q000235:genetics / Q000378:metabolism / Q000648:ultrastructure; D018506:Gene Expression Regulation, Plant; D006706:Homeostasis; D006863:Hydrogen-Ion Concentration; D015151:Immunoblotting; D018613:Microscopy, Confocal; D046529:Microscopy, Electron, Transmission; D009154:Mutation; D009995:Osmosis; D010788:Photosynthesis / Q000235:genetics; D045322:Photosynthetic Reaction Center Complex Proteins / Q000235:genetics / Q000378:metabolism; D010802:Phylogeny; D018515:Plant Leaves / Q000235:genetics / Q000378:metabolism; D030821:Plants, Genetically Modified; D018087:Plastids / Q000235:genetics / Q000378:metabolism* / Q000648:ultrastructure; D027961:Potassium-Hydrogen Antiporters / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D020524:Thylakoids / Q000737:chemistry / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; C000589493:KEA1 protein, Arabidopsis; D045322:Photosynthetic Reaction Center Complex Proteins; D027961:Potassium-Hydrogen Antiporters; C501258:potassium transporter, Arabidopsis; D002734:Chlorophyll