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The Tomato SlVIPP1 Gene Is Required for Plant Survival Through the Proper Development of Chloroplast Thylakoid Membrane

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The Tomato SlVIPP1 Gene Is Required for Plant Survival Through the Proper Development of Chloroplast Thylakoid Membrane

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dc.contributor.author Micol-Ponce, Rosa es_ES
dc.contributor.author García-Alcázar, Manuel es_ES
dc.contributor.author Capel, Carmen es_ES
dc.contributor.author Yuste-Lisbona, Fernando Juan es_ES
dc.contributor.author Pineda Chaza, Benito José es_ES
dc.contributor.author Atarés Huerta, Alejandro es_ES
dc.contributor.author García Sogo, Begoña es_ES
dc.contributor.author Capel, Juan es_ES
dc.contributor.author Moreno Ferrero, Vicente es_ES
dc.contributor.author Lozano, Rafael es_ES
dc.date.accessioned 2021-05-08T03:31:21Z
dc.date.available 2021-05-08T03:31:21Z
dc.date.issued 2020-08-26 es_ES
dc.identifier.uri http://hdl.handle.net/10251/166079
dc.description.abstract [EN] Since membranes play essential roles in all living beings, all cells have developed mechanisms for efficient and fast repair of membrane damage. InEscherichia coli, the Phage shock stress A (PspA) protein is involved in the maintenance of the integrity of its inner membrane in response to the damage produced by exposure to stress conditions. A role in thylakoid membrane maintenance and reorganization has been proposed for Vesicle Inducing Protein in Plastid 1 (VIPP1), the putative PspA ortholog inArabidopsis thaliana. While some membranes of plant cells have been extensively studied, the biosynthesis and maintenance of chloroplast thylakoid membrane remains poorly known. Here, we report the cloning and functional characterization of the tomato (Solanum lycopersicumL.) ortholog ofEscherichia coli PspAandArabidopsis thaliana VIPP1, which we dubbedSlVIPP1. Our genetic and molecular characterization ofslvipp1, an insertional mutant, allowed us to conclude that the tomatoSlVIPP1gene is needed for development, as ArabidopsisVIPP1, but notEscherichia coli PspA. Homozygousslvipp1tomato plants are albino and exhibit early lethality and highly aberrant chloroplast development with almost complete absence of thylakoids. The phenotype of tomato RNAi lines and that of additionalslvipp1alleles generated by CRISPR/Cas9 gene editing technology confirmed that the morphological and histological aberrations shown byslvipp1homozygotes are caused byVIPP1lack of function. We also found that tomatoSlVIPP1overexpression does not cause any visible effect on plant morphology and viability. Our work withslvipp1plants evidences thatSlVIPP1is an essential gene required for tomato survival, since its function is crucial for the proper formation and/or maintenance of thylakoid membranes. es_ES
dc.description.sponsorship This work was supported by research grants from the Spanish Ministry of Science and Innovation and the UE-European Regional Development Fund (grants PID2019-110833RB-C31 and PID2019-110833RB-C32) and the Research and Innovation Programme of the European Union Horizon 2020 (BRESOV Project, ID 774244). A PhD fellowship to MG-A was funded by the FPU Programme of the Spanish Ministry of Science and Innovation. The authors thank research facilities provided by the Campus de Excelencia Internacional Agroalimentario (CeiA3). es_ES
dc.language Inglés es_ES
dc.publisher Frontiers Media SA es_ES
dc.relation.ispartof Frontiers in Plant Science es_ES
dc.rights Reconocimiento (by) es_ES
dc.subject SlVIPP1 es_ES
dc.subject Tomato es_ES
dc.subject Chloroplast es_ES
dc.subject Thylakoid membrane es_ES
dc.subject PspA es_ES
dc.subject Albinism es_ES
dc.subject Lethality es_ES
dc.subject.classification GENETICA es_ES
dc.title The Tomato SlVIPP1 Gene Is Required for Plant Survival Through the Proper Development of Chloroplast Thylakoid Membrane es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.3389/fpls.2020.01305 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/774244/EU/Breeding for Resilient, Efficient and Sustainable Organic Vegetable production/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-110833RB-C31/ES/REGULACION GENETICA DE LA ACTIVIDAD DE LOS MERISTEMOS REPRODUCTIVOS Y SU PAPEL EN LA MEJORA DE LA PRODUCTIVIDAD DE TOMATE/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-110833RB-C32/ES/EDICION DE PROMOTORES DE GENES QUE REGULAN EL DESARROLLO REPRODUCTIVO EN TOMATE COMO ESTRATEGIA PARA MANTENER LA PRODUCCION EN CONDICIONES DE ESTRES ABIOTICO/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Departamento de Biotecnología - Departament de Biotecnologia es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes es_ES
dc.description.bibliographicCitation Micol-Ponce, R.; García-Alcázar, M.; Capel, C.; Yuste-Lisbona, FJ.; Pineda Chaza, BJ.; Atarés Huerta, A.; García Sogo, B.... (2020). The Tomato SlVIPP1 Gene Is Required for Plant Survival Through the Proper Development of Chloroplast Thylakoid Membrane. Frontiers in Plant Science. 11:1-14. https://doi.org/10.3389/fpls.2020.01305 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.3389/fpls.2020.01305 es_ES
dc.description.upvformatpinicio 1 es_ES
dc.description.upvformatpfin 14 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 11 es_ES
dc.identifier.eissn 1664-462X es_ES
dc.identifier.pmid 32983195 es_ES
dc.identifier.pmcid PMC7479267 es_ES
dc.relation.pasarela S\423097 es_ES
dc.contributor.funder European Commission es_ES
dc.contributor.funder Agencia Estatal de Investigación es_ES
dc.contributor.funder Ministerio de Ciencia e Innovación es_ES
dc.description.references Adikusuma, F., Piltz, S., Corbett, M. A., Turvey, M., McColl, S. R., Helbig, K. J., … Thomas, P. Q. (2018). Large deletions induced by Cas9 cleavage. Nature, 560(7717), E8-E9. doi:10.1038/s41586-018-0380-z es_ES
dc.description.references Altschul, S. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389-3402. doi:10.1093/nar/25.17.3389 es_ES
dc.description.references Aseeva, E., Ossenbühl, 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(2), 119-128. doi:10.1016/j.plaphy.2007.01.005 es_ES
dc.description.references Babu, M. M. (2016). The contribution of intrinsically disordered regions to protein function, cellular complexity, and human disease. Biochemical Society Transactions, 44(5), 1185-1200. doi:10.1042/bst20160172 es_ES
dc.description.references Brinkman, E. K., Chen, T., Amendola, M., & van Steensel, B. (2014). Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Research, 42(22), e168-e168. doi:10.1093/nar/gku936 es_ES
dc.description.references Brissette, J. L., Russel, M., Weiner, L., & Model, P. (1990). Phage shock protein, a stress protein of Escherichia coli. Proceedings of the National Academy of Sciences, 87(3), 862-866. doi:10.1073/pnas.87.3.862 es_ES
dc.description.references Ellul, P., Garcia-Sogo, B., Pineda, B., Ríos, G., Roig, L., & Moreno, V. (2003). The ploidy level of transgenic plants in Agrobacterium-mediated transformation of tomato cotyledons (Lycopersicon esculentum L.Mill.) is genotype and procedure dependent. Theoretical and Applied Genetics, 106(2), 231-238. doi:10.1007/s00122-002-0928-y es_ES
dc.description.references Flores-Kim, J., & Darwin, A. J. (2016). The Phage Shock Protein Response. Annual Review of Microbiology, 70(1), 83-101. doi:10.1146/annurev-micro-102215-095359 es_ES
dc.description.references 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(21), 4620-4628. doi:10.1091/mbc.e09-04-0319 es_ES
dc.description.references Gao, H., & Xu, X. (2009). Depletion of Vipp1 inSynechocystissp. PCC 6803 affects photosynthetic activity before the loss of thylakoid membranes. FEMS Microbiology Letters, 292(1), 63-70. doi:10.1111/j.1574-6968.2008.01470.x es_ES
dc.description.references Gao, F., Chen, B., Jiao, J., Jia, L., & Liu, C. (2017). Two Novel Vesicle-Inducing Proteins in Plastids 1 Genes Cloned and Characterized in Triticum urartu. PLOS ONE, 12(1), e0170439. doi:10.1371/journal.pone.0170439 es_ES
dc.description.references García-Alcázar, M., Giménez, E., Pineda, B., Capel, C., García-Sogo, B., Sánchez, S., … Lozano, R. (2017). Albino T-DNA tomato mutant reveals a key function of 1-deoxy-D-xylulose-5-phosphate synthase (DXS1) in plant development and survival. Scientific Reports, 7(1). doi:10.1038/srep45333 es_ES
dc.description.references Gerdes, L., Bals, T., Klostermann, E., Karl, M., Philippar, K., Hünken, M., … Schünemann, D. (2006). A Second Thylakoid Membrane-localized Alb3/OxaI/YidC Homologue Is Involved in Proper Chloroplast Biogenesis in Arabidopsis thaliana. Journal of Biological Chemistry, 281(24), 16632-16642. doi:10.1074/jbc.m513623200 es_ES
dc.description.references Giménez, E., Pineda, B., Capel, J., Antón, M. T., Atarés, A., Pérez-Martín, F., … Lozano, R. (2010). Functional Analysis of the Arlequin Mutant Corroborates the Essential Role of the ARLEQUIN/TAGL1 Gene during Reproductive Development of Tomato. PLoS ONE, 5(12), e14427. doi:10.1371/journal.pone.0014427 es_ES
dc.description.references Gleave, A. P. (1992). A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Molecular Biology, 20(6), 1203-1207. doi:10.1007/bf00028910 es_ES
dc.description.references Heidrich, J., Thurotte, A., & Schneider, D. (2017). Specific interaction of IM30/Vipp1 with cyanobacterial and chloroplast membranes results in membrane remodeling and eventually in membrane fusion. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1859(4), 537-549. doi:10.1016/j.bbamem.2016.09.025 es_ES
dc.description.references Hennig, R., Heidrich, J., Saur, M., Schmüser, L., Roeters, S. J., Hellmann, N., … Schneider, D. (2015). IM30 triggers membrane fusion in cyanobacteria and chloroplasts. Nature Communications, 6(1). doi:10.1038/ncomms8018 es_ES
dc.description.references Hennig, R., West, A., Debus, M., Saur, M., Markl, J., Sachs, J. N., & Schneider, D. (2017). The IM30/Vipp1 C-terminus associates with the lipid bilayer and modulates membrane fusion. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1858(2), 126-136. doi:10.1016/j.bbabio.2016.11.004 es_ES
dc.description.references Ishida, T., & Kinoshita, K. (2007). PrDOS: prediction of disordered protein regions from amino acid sequence. Nucleic Acids Research, 35(Web Server), W460-W464. doi:10.1093/nar/gkm363 es_ES
dc.description.references Jarvis, P., & Robinson, C. (2004). Mechanisms of Protein Import and Routing in Chloroplasts. Current Biology, 14(24), R1064-R1077. doi:10.1016/j.cub.2004.11.049 es_ES
dc.description.references Joly, N., Engl, C., Jovanovic, G., Huvet, M., Toni, T., Sheng, X., … Buck, M. (2010). Managing membrane stress: the phage shock protein (Psp) response, from molecular mechanisms to physiology. FEMS Microbiology Reviews, 34(5), 797-827. doi:10.1111/j.1574-6976.2010.00240.x es_ES
dc.description.references Jovanovic, G., Weiner, L., & Model, P. (1996). Identification, nucleotide sequence, and characterization of PspF, the transcriptional activator of the Escherichia coli stress-induced psp operon. Journal of Bacteriology, 178(7), 1936-1945. doi:10.1128/jb.178.7.1936-1945.1996 es_ES
dc.description.references Junglas, B., Siebenaller, C., Schlösser, L., Hellmann, N., & Schneider, D. (2020). GTP hydrolysis by Synechocystis IM30 does not decisively affect its membrane remodeling activity. Scientific Reports, 10(1). doi:10.1038/s41598-020-66818-9 es_ES
dc.description.references 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, 98(7), 4238-4242. doi:10.1073/pnas.061500998 es_ES
dc.description.references Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33(7), 1870-1874. doi:10.1093/molbev/msw054 es_ES
dc.description.references Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., … Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23(21), 2947-2948. doi:10.1093/bioinformatics/btm404 es_ES
dc.description.references Li, H., Kaneko, Y., & Keegstra, K. (1994). Molecular cloning of a chloroplastic proteinassociated with both the envelope and thylakoid membranes. Plant Molecular Biology, 25(4), 619-632. doi:10.1007/bf00029601 es_ES
dc.description.references LICHTENTHALER, H. K., & WELLBURN, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 11(5), 591-592. doi:10.1042/bst0110591 es_ES
dc.description.references Mechela, A., Schwenkert, S., & Soll, J. (2019). A brief history of thylakoid biogenesis. Open Biology, 9(1), 180237. doi:10.1098/rsob.180237 es_ES
dc.description.references Myburg, A. A., Grattapaglia, D., Tuskan, G. A., Hellsten, U., Hayes, R. D., Grimwood, J., … Bauer, D. (2014). The genome of Eucalyptus grandis. Nature, 510(7505), 356-362. doi:10.1038/nature13308 es_ES
dc.description.references Myouga, F., Akiyama, K., Tomonaga, Y., Kato, A., Sato, Y., Kobayashi, M., … Shinozaki, K. (2013). The Chloroplast Function Database II: A Comprehensive Collection of Homozygous Mutants and Their Phenotypic/Genotypic Traits for Nuclear-Encoded Chloroplast Proteins. Plant and Cell Physiology, 54(2), e2-e2. doi:10.1093/pcp/pcs171 es_ES
dc.description.references 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. The Plant Cell, 24(2), 637-659. doi:10.1105/tpc.111.092692 es_ES
dc.description.references Ohnishi, N., Zhang, L., & Sakamoto, W. (2018). VIPP1 Involved in Chloroplast Membrane Integrity Has GTPase Activity in Vitro. Plant Physiology, 177(1), 328-338. doi:10.1104/pp.18.00145 es_ES
dc.description.references Oliveros, J. C., Franch, M., Tabas-Madrid, D., San-León, D., Montoliu, L., Cubas, P., & Pazos, F. (2016). Breaking-Cas—interactive design of guide RNAs for CRISPR-Cas experiments for ENSEMBL genomes. Nucleic Acids Research, 44(W1), W267-W271. doi:10.1093/nar/gkw407 es_ES
dc.description.references Pérez-Martín, F., Yuste-Lisbona, F. J., Pineda, B., Angarita-Díaz, M. P., García-Sogo, B., Antón, T., … Lozano, R. (2017). A collection of enhancer trap insertional mutants for functional genomics in tomato. Plant Biotechnology Journal, 15(11), 1439-1452. doi:10.1111/pbi.12728 es_ES
dc.description.references Pérez-Martín, F., Yuste-Lisbona, F. J., Pineda, B., García-Sogo, B., Olmo, I. del, de Dios Alché, J., … Lozano, R. (2018). Developmental role of the tomato Mediator complex subunit MED18 in pollen ontogeny. The Plant Journal, 96(2), 300-315. doi:10.1111/tpj.14031 es_ES
dc.description.references Rodríguez-Leal, D., Lemmon, Z. H., Man, J., Bartlett, M. E., & Lippman, Z. B. (2017). Engineering Quantitative Trait Variation for Crop Improvement by Genome Editing. Cell, 171(2), 470-480.e8. doi:10.1016/j.cell.2017.08.030 es_ES
dc.description.references Shin, H. Y., Wang, C., Lee, H. K., Yoo, K. H., Zeng, X., Kuhns, T., … Hennighausen, L. (2017). CRISPR/Cas9 targeting events cause complex deletions and insertions at 17 sites in the mouse genome. Nature Communications, 8(1). doi:10.1038/ncomms15464 es_ES
dc.description.references Srivastava, R., Pisareva, T., & Norling, B. (2005). Proteomic studies of the thylakoid membrane ofSynechocystis sp. PCC 6803. PROTEOMICS, 5(18), 4905-4916. doi:10.1002/pmic.200500111 es_ES
dc.description.references Srivastava, R., Battchikova, N., Norling, B., & Aro, E.-M. (2006). Plasma membrane of Synechocystis PCC 6803: a heterogeneous distribution of membrane proteins. Archives of Microbiology, 185(3), 238-243. doi:10.1007/s00203-006-0086-8 es_ES
dc.description.references Teng, Y.-S., Su, Y., Chen, L.-J., Lee, Y. J., Hwang, I., & Li, H. (2006). Tic21 Is an Essential Translocon Component for Protein Translocation across the Chloroplast Inner Envelope Membrane. The Plant Cell, 18(9), 2247-2257. doi:10.1105/tpc.106.044305 es_ES
dc.description.references Vothknecht, U. C., Otters, S., Hennig, R., & Schneider, D. (2011). Vipp1: a very important protein in plastids?! Journal of Experimental Botany, 63(4), 1699-1712. doi:10.1093/jxb/err357 es_ES
dc.description.references Wesley, S. V., Helliwell, C. A., Smith, N. A., Wang, M., Rouse, D. T., Liu, Q., … Waterhouse, P. M. (2001). Construct design for efficient, effective and high-throughput gene silencing in plants. The Plant Journal, 27(6), 581-590. doi:10.1046/j.1365-313x.2001.01105.x es_ES
dc.description.references 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, 98(7), 4243-4248. doi:10.1073/pnas.061501198 es_ES
dc.description.references Yuste-Lisbona, F. J., Fernández-Lozano, A., Pineda, B., Bretones, S., Ortíz-Atienza, A., García-Sogo, B., … Lozano, R. (2020). ENOregulates tomato fruit size through the floral meristem development network. Proceedings of the National Academy of Sciences, 117(14), 8187-8195. doi:10.1073/pnas.1913688117 es_ES
dc.description.references Zhang, L., & Sakamoto, W. (2013). Possible function of VIPP1 in thylakoids. Plant Signaling & Behavior, 8(2), e22860. doi:10.4161/psb.22860 es_ES
dc.description.references Zhang, L., & Sakamoto, W. (2015). Possible function of VIPP1 in maintaining chloroplast membranes. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1847(9), 831-837. doi:10.1016/j.bbabio.2015.02.013 es_ES
dc.description.references Zhang, L., Kato, Y., Otters, S., Vothknecht, U. C., & Sakamoto, W. (2012). Essential Role of VIPP1 in Chloroplast Envelope Maintenance in Arabidopsis  . The Plant Cell, 24(9), 3695-3707. doi:10.1105/tpc.112.103606 es_ES
dc.description.references 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(23), 15904-15914. doi:10.1074/jbc.m114.555631 es_ES
dc.description.references 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(3), 1983-1995. doi:10.1104/pp.16.00532 es_ES
dc.description.references Zouine, M., Maza, E., Djari, A., Lauvernier, M., Frasse, P., Smouni, A., … Bouzayen, M. (2017). TomExpress, a unified tomato RNA-Seq platform for visualization of expression data, clustering and correlation networks. The Plant Journal, 92(4), 727-735. doi:10.1111/tpj.13711 es_ES


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