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Envelope K+/H+ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development.
Plant Physiol. 2016 09; 172(1):441-9.PP

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.

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Authors+Show Affiliations

Aranda-Sicilia MN
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.).
Aboukila A
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.).
Armbruster U
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.).
Cagnac O
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.).
Schumann T
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.).
Kunz HH
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.).
Jahns P
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.).
Rodríguez-Rosales MP
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.).
Sze H
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.).
Venema K
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.

MeSH

Amino Acid SequenceArabidopsisArabidopsis ProteinsChlorophyllChloroplastsGene Expression Regulation, PlantHomeostasisHydrogen-Ion ConcentrationImmunoblottingMicroscopy, ConfocalMicroscopy, Electron, TransmissionMutationOsmosisPhotosynthesisPhotosynthetic Reaction Center Complex ProteinsPhylogenyPlant LeavesPlants, Genetically ModifiedPlastidsPotassium-Hydrogen AntiportersThylakoids

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

27443603

Citation

Aranda-Sicilia, María Nieves, et al. "Envelope K+/H+ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development." Plant Physiology, vol. 172, no. 1, 2016, pp. 441-9.
Aranda-Sicilia MN, Aboukila A, Armbruster U, et al. Envelope K+/H+ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development. Plant Physiol. 2016;172(1):441-9.
Aranda-Sicilia, M. N., Aboukila, A., Armbruster, U., Cagnac, O., Schumann, T., Kunz, H. H., Jahns, P., Rodríguez-Rosales, M. P., Sze, H., & Venema, K. (2016). Envelope K+/H+ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development. Plant Physiology, 172(1), 441-9. https://doi.org/10.1104/pp.16.00995
Aranda-Sicilia MN, et al. Envelope K+/H+ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development. Plant Physiol. 2016;172(1):441-9. PubMed PMID: 27443603.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Envelope K+/H+ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development. AU - Aranda-Sicilia,María Nieves, AU - Aboukila,Ali, AU - Armbruster,Ute, AU - Cagnac,Olivier, AU - Schumann,Tobias, AU - Kunz,Hans-Henning, AU - Jahns,Peter, AU - Rodríguez-Rosales,María Pilar, AU - Sze,Heven, AU - Venema,Kees, Y1 - 2016/07/21/ PY - 2016/06/21/received PY - 2016/07/19/accepted PY - 2016/7/23/entrez PY - 2016/7/23/pubmed PY - 2017/9/28/medline SP - 441 EP - 9 JF - Plant physiology JO - Plant Physiol VL - 172 IS - 1 N2 - 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. SN - 1532-2548 UR - https://www.unboundmedicine.com/medline/citation/27443603/Envelope_K+/H+_Antiporters_AtKEA1_and_AtKEA2_Function_in_Plastid_Development_ DB - PRIME DP - Unbound Medicine ER -