VIPP2 interacts with VIPP1 and HSP22E/F at chloroplast membranes and modulates a retrograde signal for HSP22E/F gene expression.
Chlamydomonas reinhardtii
/ genetics
Chlorophyceae
/ genetics
Chloroplasts
/ metabolism
Cloning, Molecular
Gene Expression Regulation, Plant
Immunoprecipitation
Mass Spectrometry
Membrane Proteins
/ metabolism
Microscopy, Electron, Transmission
Microscopy, Fluorescence
Phylogeny
Plant Proteins
/ metabolism
Recombinant Proteins
Thylakoids
/ metabolism
high light response
membrane stress
molecular chaperones
protein homeostasis
reactive oxygen species
retrograde signalling
thylakoid membrane biogenesis
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
13
07
2018
revised:
22
01
2020
accepted:
23
01
2020
pubmed:
30
1
2020
medline:
28
1
2021
entrez:
30
1
2020
Statut:
ppublish
Résumé
VIPP proteins aid thylakoid biogenesis and membrane maintenance in cyanobacteria, algae, and plants. Some members of the Chlorophyceae contain two VIPP paralogs termed VIPP1 and VIPP2, which originate from an early gene duplication event during the evolution of green algae. VIPP2 is barely expressed under nonstress conditions but accumulates in cells exposed to high light intensities or H
Substances chimiques
Membrane Proteins
0
Plant Proteins
0
Recombinant Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1212-1229Informations de copyright
© 2020 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.
Références
Abulimiti, A., Qiu, X., Chen, J., Liu, Y., & Chang, Z. (2003). Reversible methionine sulfoxidation of Mycobacterium tuberculosis small heat shock protein Hsp16.3 and its possible role in scavenging oxidants. Biochemical and Biophysical Research Communications, 305, 87-93.
Allorent, G., & Petroutsos, D. (2017). Photoreceptor-dependent regulation of photoprotection. Current Opinion in Plant Biology, 37, 102-108.
Asamizu, E., Miura, K., Kucho, K., Inoue, Y., Fukuzawa, H., Ohyama, K., … Tabata, S. (2000). Generation of expressed sequence tags from low-CO2 and high-CO2 adapted cells of Chlamydomonas reinhardtii. DNA Research, 7, 305-307.
Aseeva, E., Ossenbuhl, F., Eichacker, L. A., Wanner, G., Soll, J., & Vothknecht, U. C. (2004). Complex formation of Vipp1 depends on its alpha-helical PspA-like domain. Journal of Biological Chemistry, 279, 35535-35541.
Aseeva, E., Ossenbuhl, F., Sippel, C., Cho, W. K., Stein, B., Eichacker, L. A., … Vothknecht, U. C. (2007). Vipp1 is required for basic thylakoid membrane formation but not for the assembly of thylakoid protein complexes. Plant Physiology and Biochemistry, 45, 119-128.
Attard, G. S., Templer, R. H., Smith, W. S., Hunt, A. N., & Jackowski, S. (2000). Modulation of CTP:phosphocholine cytidylyltransferase by membrane curvature elastic stress. Proceedings of the National Academy of Sciences of the United States of America, 97, 9032-9036.
Bellafiore, S., Ferris, P., Naver, H., Gohre, V., & Rochaix, J. D. (2002). Loss of Albino3 leads to the specific depletion of the light-harvesting system. Plant Cell, 14, 2303-2314.
Bernfur, K., Rutsdottir, G., & Emanuelsson, C. (2017). The chloroplast-localized small heat shock protein Hsp21 associates with the thylakoid membranes in heat-stressed plants. Protein Science, 26, 1773-1784.
Bryan, S. J., Burroughs, N. J., Shevela, D., Yu, J., Rupprecht, E., Liu, L. N., … Mullineaux, C. W. (2014). Localisation and interactions of the Vipp1 protein in cyanobacteria. Molecular Microbiology., 94, 1179-1195.
Chang, H. L., Tseng, Y. L., Ho, K. L., Shie, S. C., Wu, P. S., Hsu, Y. T., & Lee, T. M. (2014). Reactive oxygen species modulate the differential expression of methionine sulfoxide reductase genes in Chlamydomonas reinhardtii under high light illumination. Physiologia Plantarum, 150, 550-564.
Chen, S. T., He, N. Y., Chen, J. H., & Guo, F. Q. (2017). Identification of core subunits of photosystem II as action sites of HSP21, which is activated by the GUN5-mediated retrograde pathway in Arabidopsis. Plant Journal, 89, 1106-1118.
Cox, J., Hein, M. Y., Luber, C. A., Paron, I., Nagaraj, N., & Mann, M. (2014). MaxLFQ allows accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction. Molecular & Cellular Proteomics., 13, 2513-2526.
Cox, J., & Mann, M. (2008). MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature Biotechnology, 26, 1367-1372.
Crozet, P., Navarro, F. J., Willmund, F., Mehrshahi, P., Bakowski, K., Lauersen, K. J., … Lemaire, S. D. (2018). Birth of a photosynthetic chassis: A MoClo toolkit enabling synthetic biology in the microalga Chlamydomonas reinhardtii. ACS Synthetic Biology, 7, 2074-2086.
DeLisa, M. P., Lee, P., Palmer, T., & Georgiou, G. (2004). Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway. Journal of Bacteriology, 186, 366-373.
Engl, C., Jovanovic, G., Lloyd, L. J., Murray, H., Spitaler, M., Ying, L., … Buck, M. (2009). In vivo localizations of membrane stress controllers PspA and PspG in Escherichia coli. Molecular Microbiology, 73, 382-396.
Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39, 783-791.
Fuhrmann, E., Bultema, J. B., Kahmann, U., Rupprecht, E., Boekema, E. J., & Schneider, D. (2009). The vesicle-inducing protein 1 from Synechocystis sp. PCC 6803 organizes into diverse higher-ordered ring structures. Molecular Biology of the Cell, 20, 4620-4628.
Fuhrmann, E., Gathmann, S., Rupprecht, E., Golecki, J., & Schneider, D. (2009). Thylakoid membrane reduction affects the photosystem stoichiometry in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiology, 149, 735-744.
Gao, F., Wang, W., Zhang, W., & Liu, C. (2015). Alpha-helical domains affecting the oligomerization of Vipp1 and its interaction with Hsp70/DnaK in Chlamydomonas. Biochemistry, 54, 4877-4889.
Gao, H., & Xu, X. (2009). Depletion of Vipp1 in Synechocystis sp. PCC 6803 affects photosynthetic activity before the loss of thylakoid membranes. FEMS Microbiology Letters, 292, 63-70.
Gautier, R., Douguet, D., Antonny, B., & Drin, G. (2008). HELIQUEST: A web server to screen sequences with specific α-helical properties. Bioinformatics, 24, 2101-2102.
Göhre, V., Ossenbuhl, F., Crevecoeur, M., Eichacker, L. A., & Rochaix, J. D. (2006). One of two alb3 proteins is essential for the assembly of the photosystems and for cell survival in Chlamydomonas. Plant Cell, 18, 1454-1466.
Gustavsson, N., Kokke, B. P., Harndahl, U., Silow, M., Bechtold, U., Poghosyan, Z., … Sundby, C. (2002). A peptide methionine sulfoxide reductase highly expressed in photosynthetic tissue in Arabidopsis thaliana can protect the chaperone-like activity of a chloroplast-localized small heat shock protein. Plant Journal, 29, 545-553.
Gutu, A., Chang, F., & O'Shea, E. K. (2018). Dynamical localization of a thylakoid membrane binding protein is required for acquisition of photosynthetic competency. Molecular Microbiology., 108, 16-31.
Hankamer, B. D., Elderkin, S. L., Buck, M., & Nield, J. (2004). Organization of the AAA(+) adaptor protein PspA is an oligomeric ring. Journal of Biological Chemistry, 279, 8862-8866.
Harndahl, U., Hall, R. B., Osteryoung, K. W., Vierling, E., Bornman, J. F., & Sundby, C. (1999). The chloroplast small heat shock protein undergoes oxidation-dependent conformational changes and may protect plants from oxidative stress. Cell Stress and Chaperones, 4, 129-138.
Hemme, D., Veyel, D., Mühlhaus, T., Sommer, F., Juppner, J., Unger, A. K., … Schroda, M. (2014). Systems-wide analysis of acclimation responses to long-term heat stress and recovery in the photosynthetic model organism Chlamydomonas reinhardtii. Plant Cell, 26, 4270-4297.
Hennig, R., Heidrich, J., Saur, M., Schmuser, L., Roeters, S. J., Hellmann, N., … Schneider, D. (2015). IM30 triggers membrane fusion in cyanobacteria and chloroplasts. Nature Communications, 6, 7018.
Jovanovic, G., Mehta, P., McDonald, C., Davidson, A. C., Uzdavinys, P., Ying, L., & Buck, M. (2014). The N-terminal amphipathic helices determine regulatory and effector functions of phage shock protein A (PspA) in Escherichia coli. Journal of Molecular Biology, 426, 1498-1511.
Kindle, K. L. (1990). High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences of the United States of America, 87, 1228-1232.
Kirsten, M. L., Baron, R. A., Seabra, M. C., & Ces, O. (2013). Rab1a and Rab5a preferentially bind to binary lipid compositions with higher stored curvature elastic energy. Molecular Membrane Biology, 30, 303-314.
Kitagawa, M., Miyakawa, M., Matsumura, Y., & Tsuchido, T. (2002). Escherichia coli small heat shock proteins, IbpA and IbpB, protect enzymes from inactivation by heat and oxidants. European Journal of Biochemistry, 269, 2907-2917.
Kleerebezem, M., Crielaard, W., & Tommassen, J. (1996). Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the protonmotive force under stress conditions. EMBO Journal, 15, 162-171.
Kobayashi, R., Suzuki, T., & Yoshida, M. (2007). Escherichia coli phage-shock protein A (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Molecular Microbiology, 66, 100-109.
Kroll, D., Meierhoff, K., Bechtold, N., Kinoshita, M., Westphal, S., Vothknecht, U. C., … Westhoff, P. (2001). VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proceedings of the National Academy of Sciences of the United States of America, 98, 4238-4242.
Kropat, J., Hong-Hermesdorf, A., Casero, D., Ent, P., Castruita, M., Pellegrini, M., … Malasarn, D. (2011). A revised mineral nutrient supplement increases biomass and growth rate in Chlamydomonas reinhardtii. Plant Journal, 66, 770-780.
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870-1874.
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
Lemaire, C., & Wollman, F. A. (1989). The chloroplast ATP synthase in Chlamydomonas reinhardtii. I. Characterization of its nine constitutive subunits. Journal of Biological Chemistry, 264, 10228-10234.
Li, H. M., Kaneko, Y., & Keegstra, K. (1994). Molecular cloning of a chloroplastic protein associated with both the envelope and thylakoid membranes. Plant Molecular Biology, 25, 619-632.
Li, X., Zhang, R., Patena, W., Gang, S. S., Blum, S. R., Ivanova, N., … Jonikas, M. C. (2016). An indexed, mapped mutant library enables reverse genetics studies of biological processes in Chlamydomonas reinhardtii. Plant Cell, 28, 367-387.
Liu, C., Willmund, F., Golecki, J. R., Cacace, S., Hess, B., Markert, C., & Schroda, M. (2007). The chloroplast HSP70B-CDJ2-CGE1 chaperones catalyse assembly and disassembly of VIPP1 oligomers in Chlamydomonas. Plant Journal, 50, 265-277.
Liu, C., Willmund, F., Whitelegge, J. P., Hawat, S., Knapp, B., Lodha, M., & Schroda, M. (2005). J-domain protein CDJ2 and HSP70B are a plastidic chaperone pair that interacts with vesicle-inducing protein in plastids 1. Molecular Biology of the Cell, 16, 1165-1177.
Lo, S. M., & Theg, S. M. (2012). Role of vesicle-inducing protein in plastids 1 in cpTat transport at the thylakoid. Plant Journal, 71, 656-668.
Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 193, 265-275.
Male, A. L., Oyston, P. C. F., & Tavassoli, A. (2014). Self-assembly of Escherichia coli Phage Shock Protein A. Advances in Microbiology, 04, 353-359.
Manganelli, R., & Gennaro, M. L. (2017). Protecting from envelope stress: Variations on the Phage-Shock-Protein Theme. Trends in Microbiology, 25, 205-216.
Maruyama, S., Tokutsu, R., & Minagawa, J. (2014). Transcriptional regulation of the stress-responsive light harvesting complex genes in Chlamydomonas reinhardtii. Plant and Cell Physiology, 55, 1304-1310.
McDonald, C., Jovanovic, G., Ces, O., & Buck, M. (2015). Membrane stored curvature elastic stress modulates recruitment of maintenance proteins PspA and Vipp1. MBio, 6, e01188-e01115.
McDonald, C., Jovanovic, G., Wallace, B. A., Ces, O., & Buck, M. (2017). Structure and function of PspA and Vipp1 N-terminal peptides: Insights into the membrane stress sensing and mitigation. Biochimica et Biophysica Acta, 1859, 28-39.
Müller, N., Leroch, M., Schumacher, J., Zimmer, D., Konnel, A., Klug, K., … Hahn, M. (2018). Investigations on VELVET regulatory mutants confirm the role of host tissue acidification and secretion of proteins in the pathogenesis of Botrytis cinerea. The New Phytologist, 219, 1062-1074.
Muranaka, L. S., Rutgers, M., Bujaldon, S., Heublein, A., Geimer, S., Wollman, F. A., & Schroda, M. (2016). TEF30 interacts with photosystem II monomers and is involved in the repair of photodamaged photosystem II in Chlamydomonas reinhardtii. Plant Physiology, 170, 821-840.
Naumann, B., Busch, A., Allmer, J., Ostendorf, E., Zeller, M., Kirchhoff, H., & Hippler, M. (2007). Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii. Proteomics, 7, 3964-3979.
Nordhues, A., Schöttler, M. A., Unger, A. K., Geimer, S., Schönfelder, S., Schmollinger, S., … Schroda, M. (2012). Evidence for a role of VIPP1 in the structural organization of the photosynthetic apparatus in Chlamydomonas. Plant Cell, 24, 637-659.
Ossenbühl, F., Gohre, V., Meurer, J., Krieger-Liszkay, A., Rochaix, J. D., & Eichacker, L. A. (2004). Efficient assembly of photosystem II in Chlamydomonas reinhardtii requires Alb3.1p, a homolog of Arabidopsis ALBINO3. Plant Cell, 16, 1790-1800.
Otters, S., Braun, P., Hubner, J., Wanner, G., Vothknecht, U. C., & Chigri, F. (2013). The first alpha-helical domain of the vesicle-inducing protein in plastids 1 promotes oligomerization and lipid binding. Planta, 237, 529-540.
Peers, G., Truong, T. B., Ostendorf, E., Busch, A., Elrad, D., Grossman, A. R., … Niyogi, K. K. (2009). An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature, 462, 518-521.
Perlaza K., Toutkoushian H., Boone M., Lam M., Iwai M., Jonikas M.C., Walter P. & Ramundo S. (2019) The Mars1 kinase confers photoprotection through signaling in the chloroplast unfolded protein response. Elife, 8.
Pierre, Y., & Popot, J. L. (1993). Identification of two 4-kDa miniproteins in the cytochrome b6f complex from Chlamydomonas reinhardtii. Comptes Rendus de l'Académie Des Sciences. Série III: Sciences de la Vie, 316, 1404-1409.
Preville, X., Salvemini, F., Giraud, S., Chaufour, S., Paul, C., Stepien, G., … Arrigo, A. P. (1999). Mammalian small stress proteins protect against oxidative stress through their ability to increase glucose-6-phosphate dehydrogenase activity and by maintaining optimal cellular detoxifying machinery. Experimental Cell Research, 247, 61-78.
Ramundo, S., Casero, D., Mühlhaus, T., Hemme, D., Sommer, F., Crevecoeur, M., … Rochaix, J. D. (2014). Conditional depletion of the Chlamydomonas chloroplast ClpP protease activates nuclear genes involved in autophagy and plastid protein quality control. Plant Cell, 26, 2201-2222.
Rütgers, M., Muranaka, L. S., Mühlhaus, T., Sommer, F., Thoms, S., Schurig, J., … Schroda, M. (2017). Substrates of the chloroplast small heat shock proteins 22E/F point to thermolability as a regulative switch for heat acclimation in Chlamydomonas reinhardtii. Plant Molecular Biology, 95, 579-591.
Rütgers, M., & Schroda, M. (2013). A role of VIPP1 as a dynamic structure within thylakoid centers as sites of photosystem biogenesis? Plant Signaling & Behavior, 8, e27037.
Saitou, N., & Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406-425.
Saur, M., Hennig, R., Young, P., Rusitzka, K., Hellmann, N., Heidrich, J., … Schneider, D. (2017). A Janus-faced IM30 ring involved in thylakoid membrane fusion is assembled from IM30 tetramers. Structure, 25(1380-1390), e1385.
Schmollinger, S., Strenkert, D., & Schroda, M. (2010). An inducible artificial microRNA system for Chlamydomonas reinhardtii confirms a key role for heat shock factor 1 in regulating thermotolerance. Current Genetics, 56, 383-389.
Schroda, M., Hemme, D., & Mühlhaus, T. (2015). The Chlamydomonas heat stress response. Plant Journal, 82, 466-480.
Schroda, M., Vallon, O., Whitelegge, J. P., Beck, C. F., & Wollman, F. A. (2001). The chloroplastic GrpE homolog of Chlamydomonas: Two isoforms generated by differential splicing. Plant Cell, 13, 2823-2839.
Schroda, M., Vallon, O., Wollman, F. A., & Beck, C. F. (1999). A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of photosystem II during and after photoinhibition. Plant Cell, 11, 1165-1178.
Srivastava, R., Pisareva, T., & Norling, B. (2005). Proteomic studies of the thylakoid membrane of Synechocystis sp. PCC 6803. Proteomics, 5, 4905-4916.
Strenkert, D., Schmollinger, S., Sommer, F., Schulz-Raffelt, M., & Schroda, M. (2011). Transcription factor dependent chromatin remodeling at heat shock and copper responsive promoters in Chlamydomonas reinhardtii. Plant Cell, 23, 2285-2301.
Sundby, C., Harndahl, U., Gustavsson, N., Ahrman, E., & Murphy, D. J. (2005). Conserved methionines in chloroplasts. Biochimica et Biophysica Acta, 1703, 191-202.
Theis, J., Gupta, T. K., Klingler, J., Wan, W., Albert, S., Keller, S., … Schroda, M. (2019). VIPP1 rods engulf membranes containing phosphatidylinositol phosphates. Scientific Reports, 9, 8725.
Theis, J., Lang, J., Spaniol, B., Ferte, S., Niemeyer, J., Sommer, F., … Schroda, M. (2019). The Chlamydomonas deg1c mutant accumulates proteins involved in high light acclimation. Plant Physiology, 18m, 1480-1497.
Theis, J., & Schroda, M. (2016). Revisiting the photosystem II repair cycle. Plant Signaling & Behavior, 11, e1218587.
Uniacke, J., Colon-Ramos, D., & Zerges, W. (2011). FISH and immunofluorescence staining in Chlamydomonas. Methods in Molecular Biology, 714, 15-29.
Vrancken, K., De Keersmaeker, S., Geukens, N., Lammertyn, E., Anne, J., & Van Mellaert, L. (2007). pspA overexpression in Streptomyces lividans improves both Sec- and Tat-dependent protein secretion. Applied Microbiology and Biotechnology, 73, 1150-1157.
Walter, B., Hristou, A., Nowaczyk, M. M., & Schunemann, D. (2015). In vitro reconstitution of co-translational D1 insertion reveals a role of the cpSec-Alb3 translocase and Vipp1 in photosystem II biogenesis. Biochemical Journal, 468, 315-324.
Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M., & Barton, G. J. (2009). Jalview Version 2-A multiple sequence alignment editor and analysis workbench. Bioinformatics, 25, 1189-1191.
Weber, E., Engler, C., Gruetzner, R., Werner, S., & Marillonnet, S. (2011). A modular cloning system for standardized assembly of multigene constructs. PLoS One, 6, e16765.
Westphal, S., Heins, L., Soll, J., & Vothknecht, U. C. (2001). Vipp1 deletion mutant of Synechocystis: A connection between bacterial phage shock and thylakoid biogenesis? Proceedings of the National Academy of Sciences of the United States of America, 98, 4243-4248.
Willmund, F., & Schroda, M. (2005). HEAT SHOCK PROTEIN 90C is a bona fide Hsp90 that interacts with plastidic HSP70B in Chlamydomonas reinhardtii. Plant Physiology, 138, 2310-2322.
Wong-Ekkabut, J., Xu, Z., Triampo, W., Tang, I. M., Tieleman, D. P., & Monticelli, L. (2007). Effect of lipid peroxidation on the properties of lipid bilayers: A molecular dynamics study. Biophysical Journal, 93, 4225-4236.
Zhang, L., Kato, Y., Otters, S., Vothknecht, U. C., & Sakamoto, W. (2012). Essential role of VIPP1 in chloroplast envelope maintenance in Arabidopsis. Plant Cell, 24, 3695-3707.
Zhang, L., Kondo, H., Kamikubo, H., Kataoka, M., & Sakamoto, W. (2016). VIPP1 has a disordered C-terminal tail necessary for protecting photosynthetic membranes against stress. Plant Physiology, 171, 1983-1995.
Zhang, L., Kusaba, M., Tanaka, A., & Sakamoto, W. (2016). Protection of chloroplast membranes by VIPP1 rescues aberrant seedling development in Arabidopsis nyc1 mutant. Frontiers in Plant Science, 7, 533.
Zhang, L., & Sakamoto, W. (2013). Possible function of VIPP1 in thylakoids: Protection but not formation? Plant Signaling & Behavior, 8, e22860.
Zhang, S., Shen, G., Li, Z., Golbeck, J. H., & Bryant, D. A. (2014). Vipp1 is essential for the biogenesis of Photosystem I but not thylakoid membranes in Synechococcus sp. PCC 7002. Journal of Biological Chemistry, 289, 15904-15914.
Zuckerkandl, E., & Pauling, L. (1965). Molecules as documents of evolutionary history. Journal of Theoretical Biology, 8, 357-366.