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The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato

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The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato

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dc.contributor.author Ling, Qihua es_ES
dc.contributor.author Sadali, Najiah Mohd. es_ES
dc.contributor.author Soufi, Ziad es_ES
dc.contributor.author Zhou, Yuan es_ES
dc.contributor.author Huang, Binquan es_ES
dc.contributor.author Zeng, Yunliu es_ES
dc.contributor.author Rodriguez-Concepcion, Manuel es_ES
dc.contributor.author Jarvis, R. Paul es_ES
dc.date.accessioned 2022-11-10T19:02:40Z
dc.date.available 2022-11-10T19:02:40Z
dc.date.issued 2021-05 es_ES
dc.identifier.issn 2055-026X es_ES
dc.identifier.uri http://hdl.handle.net/10251/189607
dc.description.abstract [EN] The maturation of green fleshy fruit to become colourful and flavoursome is an important strategy for plant reproduction and dispersal. In tomato (Solanum lycopersicum) and many other species, fruit ripening is intimately linked to the biogenesis of chromoplasts, the plastids that are abundant in ripe fruit and specialized for the accumulation of carotenoid pigments. Chromoplasts develop from pre-existing chloroplasts in the fruit, but the mechanisms underlying this transition are poorly understood. Here, we reveal a role for the chloroplast-associated protein degradation (CHLORAD) proteolytic pathway in chromoplast differentiation. Knockdown of the plastid ubiquitin E3 ligase SP1, or its homologue SPL2, delays tomato fruit ripening, whereas overexpression of SP1 accelerates ripening, as judged by colour changes. We demonstrate that SP1 triggers broader effects on fruit ripening, including fruit softening, and gene expression and metabolism changes, by promoting the chloroplast-to-chromoplast transition. Moreover, we show that tomato SP1 and SPL2 regulate leaf senescence, revealing conserved functions of CHLORAD in plants. We conclude that SP1 homologues control plastid transitions during fruit ripening and leaf senescence by enabling reconfiguration of the plastid protein import machinery to effect proteome reorganization. The work highlights the critical role of chromoplasts in fruit ripening, and provides a theoretical basis for engineering crop improvements. es_ES
dc.description.sponsorship We thank E. Johnson and R. Dhaliwal for transmission electron microscopy conducted in the Sir William Dunn School of Pathology EM Facility, D. Hauton and J. McCullagh for IC¿MS conducted in the Mass Spectrometry Research Facility in the Department of Chemistry, P. Bota for GC¿MS conducted in the Department of Plant Sciences, P. Bota and R. Ross for technical assistance, P. Pulido for assistance with the pigment analysis, and M. R. Rodriguez Goberna for HPLC conducted at CRAG, Spain. This work was supported by a Khazanah-Oxford Centre for Islamic Studies Merdeka Scholarship to N.M.S., by Strategic Priority Research Program (Type-B; project number: XDB27020107), Chinese Academy of Sciences to Q.L., by the Spanish Agencia Estatal de Investigación (grants BIO2017-84041-P and BIO2017-90877-REDT) to M.R.-C., and by the Biotechnology and Biological Sciences Research Council (BBSRC; grants BB/H008039/1, BB/K018442/1, BB/N006372/1, BB/R005591/1, BB/R009333/1 and BB/R016984/1) to R.P.J. es_ES
dc.language Inglés es_ES
dc.relation.ispartof Nature Plants es_ES
dc.rights Reserva de todos los derechos es_ES
dc.title The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1038/s41477-021-00916-y es_ES
dc.relation.projectID info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2017-84041-P/ES/NUEVAS HERRAMIENTAS BIOTECNOLOGICAS PARA MEJORAR LA PRODUCCION Y EL ALMACENAJE DE VITAMINAS A Y E EN CELULAS VEGETALES/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/AEI//BIO2017-90877-REDT/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/AEI//BIO2017-84041-P//NUEVAS HERRAMIENTAS BIOTECNOLOGICAS PARA MEJORAR LA PRODUCCION Y EL ALMACENAJE DE VITAMINAS A Y E EN CELULAS VEGETALES/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/BBSRC//BB%2FR016984%2F1/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/BBSRC//BB%2FN006372%2F1/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/BBSRC//BB%2FH008039%2F1/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/BBSRC//BB%2FR005591%2F1/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/BBSRC//BB%2FR009333%2F1/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/BBSRC//BB%2FK018442%2F1/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/CAS//XDB27020107/ es_ES
dc.rights.accessRights Abierto 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 Ling, Q.; Sadali, NM.; Soufi, Z.; Zhou, Y.; Huang, B.; Zeng, Y.; Rodriguez-Concepcion, M.... (2021). The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato. Nature Plants. 7(5):1-20. https://doi.org/10.1038/s41477-021-00916-y es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1038/s41477-021-00916-y es_ES
dc.description.upvformatpinicio 1 es_ES
dc.description.upvformatpfin 20 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 7 es_ES
dc.description.issue 5 es_ES
dc.identifier.pmid 34007040 es_ES
dc.relation.pasarela S\460356 es_ES
dc.contributor.funder Chinese Academy of Sciences es_ES
dc.contributor.funder Agencia Estatal de Investigación es_ES
dc.contributor.funder Biotechnology and Biological Sciences Research Council, Reino Unido es_ES
dc.description.references Alexander, L. & Grierson, D. Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J. Exp. Bot. 53, 2039–2055 (2002). es_ES
dc.description.references Klee, H. J. & Giovannoni, J. J. Genetics and control of tomato fruit ripening and quality attributes. Annu. Rev. Genet. 45, 41–59 (2011). es_ES
dc.description.references Seymour, G. B., Ostergaard, L., Chapman, N. H., Knapp, S. & Martin, C. Fruit development and ripening. Annu. Rev. Plant Biol. 64, 219–241 (2013). es_ES
dc.description.references Llorente, B., D’Andrea, L. & Rodriguez-Concepcion, M. Evolutionary recycling of light signaling components in fleshy fruits: new insights on the role of pigments to monitor ripening. Front. Plant Sci. 7, 263 (2016). es_ES
dc.description.references Jarvis, P. & López-Juez, E. Biogenesis and homeostasis of chloroplasts and other plastids. Nat. Rev. Mol. Cell Biol. 14, 787–802 (2013). es_ES
dc.description.references Sadali, N. M., Sowden, R. G., Ling, Q. & Jarvis, R. P. Differentiation of chromoplasts and other plastids in plants. Plant Cell Rep. 38, 803–818 (2019). es_ES
dc.description.references Barsan, C. et al. Characteristics of the tomato chromoplast revealed by proteomic analysis. J. Exp. Bot. 61, 2413–2431 (2010). es_ES
dc.description.references Egea, I. et al. Chromoplast differentiation: current status and perspectives. Plant Cell Physiol. 51, 1601–1611 (2010). es_ES
dc.description.references Li, L. & Yuan, H. Chromoplast biogenesis and carotenoid accumulation. Arch. Biochem. Biophys. 539, 102–109 (2013). es_ES
dc.description.references Pesaresi, P., Mizzotti, C., Colombo, M. & Masiero, S. Genetic regulation and structural changes during tomato fruit development and ripening. Front. Plant Sci. 5, 124 (2014). es_ES
dc.description.references Barsan, C. et al. Proteomic analysis of chloroplast-to-chromoplast transition in tomato reveals metabolic shifts coupled with disrupted thylakoid biogenesis machinery and elevated energy-production components. Plant Physiol. 160, 708–725 (2012). es_ES
dc.description.references Suzuki, M. et al. Plastid proteomic analysis in tomato fruit development. PLoS ONE 10, e0137266 (2015). es_ES
dc.description.references Szymanski, J. et al. Label-free deep shotgun proteomics reveals protein dynamics during tomato fruit tissues development. Plant J. 90, 396–417 (2017). es_ES
dc.description.references Dalal, M., Chinnusamy, V. & Bansal, K. C. Isolation and functional characterization of lycopene beta-cyclase (CYC-B) promoter from Solanum habrochaites. BMC Plant Biol. 10, 61 (2010). es_ES
dc.description.references Llorente, B. et al. Synthetic conversion of leaf chloroplasts into carotenoid-rich plastids reveals mechanistic basis of natural chromoplast development. Proc. Natl Acad. Sci. USA 117, 21796–21803 (2020). es_ES
dc.description.references Pech, J. C., Bouzayen, M. & Latché, A. in Fruit Ripening: Physiology, Signaling and Genomics (eds Nath, P. & Bouzayen, M.) 28–47 (CAB International, 2014). es_ES
dc.description.references D’Andrea, L. et al. Interference with Clp protease impairs carotenoid accumulation during tomato fruit ripening. J. Exp. Bot. 69, 1557–1568 (2018). es_ES
dc.description.references D’Andrea, L. & Rodriguez-Concepcion, M. Manipulation of plastidial protein quality control components as a new strategy to improve carotenoid contents in tomato fruit. Front. Plant Sci. 10, 1071 (2019). es_ES
dc.description.references Ling, Q., Huang, W., Baldwin, A. & Jarvis, P. Chloroplast biogenesis is regulated by direct action of the ubiquitin–proteasome system. Science 338, 655–659 (2012). es_ES
dc.description.references Pan, R., Satkovich, J. & Hu, J. E3 ubiquitin ligase SP1 regulates peroxisome biogenesis in Arabidopsis. Proc. Natl. Acad. Sci. USA 113, E7307–E7316 (2016). es_ES
dc.description.references Ling, Q., Li, N. & Jarvis, P. Chloroplast ubiquitin E3 ligase SP1: does it really function in peroxisomes? Plant Physiol. 175, 586–588 (2017). es_ES
dc.description.references Ling, Q. et al. Ubiquitin-dependent chloroplast-associated protein degradation in plants. Science 363, eaav4467 (2019). es_ES
dc.description.references Jarvis, P. Targeting of nucleus-encoded proteins to chloroplasts in plants (Tansley Review). New Phytol. 179, 257–285 (2008). es_ES
dc.description.references Schnell, D. J. The TOC GTPase receptors: regulators of the fidelity, specificity and substrate profiles of the general protein import machinery of chloroplasts. Protein J. 38, 343–350 (2019). es_ES
dc.description.references Demarsy, E., Lakshmanan, A. M. & Kessler, F. Border control: selectivity of chloroplast protein import and regulation at the TOC-complex. Front. Plant Sci. 5, 483 (2014). es_ES
dc.description.references Li, H. M. & Chiu, C. C. Protein transport into chloroplasts. Annu. Rev. Plant Biol. 61, 157–180 (2010). es_ES
dc.description.references Shi, L. X. & Theg, S. M. The chloroplast protein import system: from algae to trees. Biochim. Biophys. Acta 1833, 314–331 (2013). es_ES
dc.description.references Yan, J., Campbell, J. H., Glick, B. R., Smith, M. D. & Liang, Y. Molecular characterization and expression analysis of chloroplast protein import components in tomato (Solanum lycopersicum). PLoS ONE 9, e95088 (2014). es_ES
dc.description.references Lim, P. O., Kim, H. J. & Nam, H. G. Leaf senescence. Annu. Rev. Plant Biol. 58, 115–136 (2007). es_ES
dc.description.references Hou, X., Zhang, W., Du, T., Kang, S. & Davies, W. J. Responses of water accumulation and solute metabolism in tomato fruit to water scarcity and implications for main fruit quality variables. J. Exp. Bot. 71, 1249–1264 (2020). es_ES
dc.description.references Gray, J. E., Picton, S., Giovannoni, J. J. & Grierson, D. The use of transgenic and naturally occurring mutants to understand and manipulate tomato fruit ripening. Plant Cell Environ. 17, 557–571 (1994). es_ES
dc.description.references López Camelo, A. F. & Gómez, P. A. Comparison of color indexes for tomato ripening. Hortic. Bras. 22, 534–537 (2004). es_ES
dc.description.references Batu, A. Determination of acceptable firmness and colour values of tomatoes. J. Food Eng. 61, 471–475 (2004). es_ES
dc.description.references Zeng, Y. et al. A comprehensive analysis of chromoplast differentiation reveals complex protein changes associated with plastoglobule biogenesis and remodeling of protein systems in sweet orange flesh. Plant Physiol. 168, 1648–1665 (2015). es_ES
dc.description.references Martel, C., Vrebalov, J., Tafelmeyer, P. & Giovannoni, J. J. The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol. 157, 1568–1579 (2011). es_ES
dc.description.references Pan, Y. et al. Network inference analysis identifies an APRR2-like gene linked to pigment accumulation in tomato and pepper fruits. Plant Physiol. 161, 1476–1485 (2013). es_ES
dc.description.references Rigano, M. M., Lionetti, V., Raiola, A., Bellincampi, D. & Barone, A. Pectic enzymes as potential enhancers of ascorbic acid production through the D-galacturonate pathway in Solanaceae. Plant Sci. 266, 55–63 (2018). es_ES
dc.description.references Chan, K. X., Phua, S. Y., Crisp, P., McQuinn, R. & Pogson, B. J. Learning the languages of the chloroplast: retrograde signaling and beyond. Annu. Rev. Plant Biol. 67, 25–53 (2016). es_ES
dc.description.references Zhao, X., Huang, J. & Chory, J. Unraveling the linkage between retrograde signaling and RNA metabolism in plants. Trends Plant Sci. 25, 141–147 (2020). es_ES
dc.description.references Wu, G. Z. & Bock, R. GUN control in retrograde signaling: How GENOMES UNCOUPLED proteins adjust nuclear gene expression to plastid biogenesis. Plant Cell 33, 457–474 (2021). es_ES
dc.description.references Chen, Y. et al. Formation and change of chloroplast-located plant metabolites in response to light conditions. Int. J. Mol. Sci. 19, 654 (2018). es_ES
dc.description.references Carrari, F. et al. Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiol. 142, 1380–1396 (2006). es_ES
dc.description.references Ling, Q. & Jarvis, P. Regulation of chloroplast protein import by the ubiquitin E3 ligase SP1 is important for stress tolerance in plants. Curr. Biol. 25, 2527–2534 (2015). es_ES
dc.description.references Woo, H. R., Kim, H. J., Lim, P. O. & Nam, H. G. Leaf senescence: systems and dynamics aspects. Annu. Rev. Plant Biol. 70, 347–376 (2019). es_ES
dc.description.references Wang, R., Angenent, G. C., Seymour, G. & de Maagd, R. A. Revisiting the role of master regulators in tomato ripening. Trends Plant Sci. 25, 291–301 (2020). es_ES
dc.description.references Gao, W., Liu, W., Zhao, M. & Li, W. X. NERF encodes a RING E3 ligase important for drought resistance and enhances the expression of its antisense gene NFYA5 in Arabidopsis. Nucleic Acids Res. 43, 607–617 (2015). es_ES
dc.description.references Teng, Y. S., Chan, P. T. & Li, H. M. Differential age-dependent import regulation by signal peptides. PLoS Biol. 10, e1001416 (2012). es_ES
dc.description.references Kessler, F. Chloroplast delivery by UPS. Science 338, 622–623 (2012). es_ES
dc.description.references Cheung, A. Y., McNellis, T. & Piekos, B. Maintenance of chloroplast components during chromoplast differentiation in the tomato mutant green flesh. Plant Physiol. 101, 1223–1229 (1993). es_ES
dc.description.references Dono, G. et al. Color mutations alter the biochemical composition in the San Marzano tomato fruit. Metabolites 10, 110 (2020). es_ES
dc.description.references Parry, C., Blonquist, J. M. Jr & Bugbee, B. In situ measurement of leaf chlorophyll concentration: analysis of the optical/absolute relationship. Plant Cell Environ. 37, 2508–2520 (2014). es_ES
dc.description.references Gálvez-Valdivieso, G. et al. The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. Plant Cell 21, 2143–2162 (2009). es_ES
dc.description.references Goodstein, D. M. et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178–D1186 (2012). es_ES
dc.description.references Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994). es_ES
dc.description.references Schwacke, R. et al. ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 131, 16–26 (2003). es_ES
dc.description.references Ossowski, S., Schwab, R. & Weigel, D. Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J. 53, 674–690 (2008). es_ES
dc.description.references Fernandez, A. I. et al. Flexible tools for gene expression and silencing in tomato. Plant Physiol. 151, 1729–1740 (2009). es_ES
dc.description.references Schwab, R., Ossowski, S., Riester, M., Warthmann, N. & Weigel, D. Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18, 1121–1133 (2006). es_ES
dc.description.references Karimi, M., Inze, D. & Depicker, A. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193–195 (2002). es_ES
dc.description.references Chetty, V. J. et al. Evaluation of four Agrobacterium tumefaciens strains for the genetic transformation of tomato (Solanum lycopersicum L.) cultivar Micro-Tom. Plant Cell Rep. 32, 239–247 (2013). es_ES
dc.description.references Sun, H. J., Uchii, S., Watanabe, S. & Ezura, H. A highly efficient transformation protocol for Micro-Tom, a model cultivar for tomato functional genomics. Plant Cell Physiol. 47, 426–431 (2006). es_ES
dc.description.references Koornneef, M. et al. Chromosomal instability in cell- and tissue cultures of tomato haploids and diploids. Euphytica 43, 179–186 (1989). es_ES
dc.description.references Karimi, M., De Meyer, B. & Hilson, P. Modular cloning in plant cells. Trends Plant Sci. 10, 103–105 (2005). es_ES
dc.description.references Wu, F. H. et al. Tape-Arabidopsis Sandwich - a simpler Arabidopsis protoplast isolation method. Plant Methods 5, 16 (2009). es_ES
dc.description.references Kasmati, A. R., Töpel, M., Patel, R., Murtaza, G. & Jarvis, P. Molecular and genetic analyses of Tic20 homologues in Arabidopsis thaliana chloroplasts. Plant J. 66, 877–889 (2011). es_ES
dc.description.references Hobson, G. E., Adams, P. & Dixon, T. J. Assessing the color of tomato fruit during ripening. J. Sci. Food Agric. 34, 286–292 (1983). es_ES
dc.description.references Pathare, P. B., Opara, U. L. & Al-Said, F. A. Colour measurement and analysis in fresh and processed foods: a review. Food Bioproc. Tech. 6, 36–60 (2013). es_ES
dc.description.references Arazuri, S., Jarén, C., Arana, J. I. & de Ciriza, J. P. Influence of mechanical harvest on the physical properties of processing tomato (Lycopersicon esculentum Mill.). J. Food Eng. 80, 190–198 (2007). es_ES
dc.description.references Walsby-Tickle, J. et al. Anion-exchange chromatography mass spectrometry provides extensive coverage of primary metabolic pathways revealing altered metabolism in IDH1 mutant cells. Commun. Biol. 3, 247 (2020). es_ES
dc.description.references Lisec, J., Schauer, N., Kopka, J., Willmitzer, L. & Fernie, A. R. Corrigendum: Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 10, 1457 (2015). es_ES
dc.description.references Aronsson, H. et al. Nucleotide binding and dimerization at the chloroplast pre-protein import receptor, atToc33, are not essential in vivo but do increase import efficiency. Plant J. 63, 297–311 (2010). es_ES
dc.description.references Faurobert, M., Pelpoir, E. & Chaib, J. Phenol extraction of proteins for proteomic studies of recalcitrant plant tissues. Methods Mol. Biol. 355, 9–14 (2007). es_ES
dc.description.references Kovacheva, S. et al. In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J. 41, 412–428 (2005). es_ES
dc.description.references Kovacheva, S., Bédard, J., Wardle, A., Patel, R. & Jarvis, P. Further in vivo studies on the role of the molecular chaperone, Hsp93, in plastid protein import. Plant J. 50, 364–379 (2007). es_ES
dc.description.references Huang, W., Ling, Q., Bédard, J., Lilley, K. & Jarvis, P. In vivo analyses of the roles of essential Omp85-related proteins in the chloroplast outer envelope membrane. Plant Physiol. 157, 147–159 (2011). es_ES
dc.description.references Suorsa, M. & Aro, E. M. Expression, assembly and auxiliary functions of photosystem II oxygen-evolving proteins in higher plants. Photosynth. Res. 93, 89–100 (2007). es_ES
dc.description.references Andersen, B., Koch, B. & Scheller, H. V. Structural and functional analysis of the reducing side of photosystem I. Physiol. Plant. 84, 154–161 (1992). es_ES
dc.description.references Luo, T. et al. Distinct carotenoid and flavonoid accumulation in a spontaneous mutant of Ponkan (Citrus reticulata Blanco) results in yellowish fruit and enhanced postharvest resistance. J. Agric. Food Chem. 63, 8601–8614 (2015). es_ES
dc.description.references Li, W. et al. Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelle’s dynamics and signaling. PLoS ONE 3, e1487 (2008). es_ES
dc.description.references Hruz, T. et al. Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinformatics 2008, 420747 (2008). es_ES


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