Plastid proteomic analysis in tomato fruit development

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Suzuki, Miho ^a,b   Takahashi, Sachiko ^a   Kondo, Takanori ^a   Dohra, Hideo ^a   Ito, Yumihiko ^a   Kiriiwa, Yoshikazu ^a   Hayashi, Marina ^a   Kamiya, Shiori ^a   Kato, Masaya ^a   Fujiwara, Masayuki ^b   Fukao, Yoichiro ^b   Kobayashi, Megumi ^c   Nagata, Noriko ^c   Motohashi, Reiko ^a  

^a SHIZUOKA UNIVERSITY   (Japan)

^b NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^c JAPAN WOMEN'S UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CAROTENOID; FLAVONOID; HAIRPIN BINDING PROTEIN 1; LIPOCALIN; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; PLANT PROTEIN;

APOPTOSIS; ARABIDOPSIS; ARTICLE; CELL GROWTH; CELL METABOLISM; CELLULAR DISTRIBUTION; CHLOROPLAST; CHROMOPLAST; DEVELOPMENTAL STAGE; ENVIRONMENTAL STRESS; FRUIT COLOR; FRUIT DEVELOPMENT; IMMUNE RESPONSE; MEMBRANE STRUCTURE; NONHUMAN; PHOTOSYNTHESIS; PROTEOMICS; TOMATO; CYTOLOGY; FRUIT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PIGMENTATION; PLASTID;

CAROTENOIDS; CHLOROPLASTS; FLAVONOIDS; FRUIT; LYCOPERSICON ESCULENTUM; PIGMENTATION; PLANT PROTEINS; PLASTIDS; PROTEOMICS;

EID: 84945952781     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137266     Document Type: Article

References (67)

1. Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, et al. Chloroplast proteomics and the compartmentation of plastidial isoprenoid biosynthetic pathways. Mol Plant 2009; 2: 1154-1180. doi: 10.1093/mp/ssp088 PMID: 19969518
2. Ferro M, Brugière S, Salvi D, Seigneurin-Berny D, Court M, Moyet L, et al. AT-CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 2010; 9: 1063-1084. doi: 10.1074/mcp.M900325-MCP200 PMID: 20061580
3. Motohashi R, Rödiger A, Agne B, Baerenfaller K, Baginsky S. Common and specific protein accumulation patterns in different albino/pale-green mutants reveals regulon organization at the proteome level. Plant Physiol. 2012; 160: 2189-2201. doi: 10.1104/pp.112.204032 PMID: 23027667
4. Behrens C, Blume C, Senkler M, Eubel H, Peterhänsel C, Braun HP. The 'protein complex proteome' of chloroplasts in Arabidopsis thaliana. J Proteomics 2013; 91C: 73-83.
5. Komatsu S, Konishi H, Shen S, Yang G. Rice proteomics Mol Cell Proteomics 2003; 2.1: 2-10.
6. von Zychlinski A, Kleffmann T, Krishnamurthy N, Sjolander K, Baginsky S, Gruissem W. Proteome analysis of the rice etioplast: Metabolic and regulatory networks and novel protein functions. Mol Cell Proteomics 2005; 4: 1072-1084. PMID: 15901827
7. Baginsky S, Siddique A, Gruissem W. Proteome analysis of tobacco bright yellow-2 (BY-2) cell culture plastids as a model for undifferentiated heterotrophic plastids. J Proteome Res. 2004; 3: 1128-1137. PMID: 15595721
8. Balmer Y, Vensel WH, DuPont FM, Buchanan BB, Hurkman WJ. Proteome of amyloplasts isolated from developing wheat endosperm presents evidence of broad metabolic capability. J Exp Bot. 2006; 57: 1591-1602. PMID: 16595579
9. Stensballe A, Hald S, Bauw G, Blennow A, Welinder KG. The amyloplast proteome of potato tuber. FEBS J. 2008; 275: 1723-1741. doi: 10.1111/j.1742-4658.2008.06332.x PMID: 18331355
10. Siddique MA, Grossmann J, Gruissem W, Baginsky S. Proteome analysis of bell pepper (Capsicum annuum L.) chromoplasts. Plant Cell Physiol. 2006; 47: 1663-1673. PMID: 17098784
11. Barsan C, Sanchez-Bel P, Rombaldi C, Egea I, Rossignol M, Kuntz M, et al. Characteristics of the tomato chromoplast revealed by proteomic analysis. J Exp Bot. 2010; 61: 2413-2431. doi: 10.1093/jxb/erq070 PMID: 20363867
12. Barsan C, Zouine M, Maza E, Bian W, Egea I, Rossignol M, et al. Proteomic analysis of chloroplast-Tochromoplast transition in tomato reveals metabolic shifts coupled with disrupted thylakoid biogenesis machinery and elevated energy-production components. Plant Physiol. 2012; 160: 708-725. doi: 10. 1104/pp.112.203679 PMID: 22908117
13. Zeng Y, Pan Z, Ding Y, Zhu A, Cao H, Xu Q, et al. A proteomic analysis of the chromoplasts isolated from sweet orange fruits [Citrus sinensis (L.) Osbeck]. Journal of Experimental Botany 2011; 62: 5297-5309. doi: 10.1093/jxb/err140 PMID: 21841170
14. Wang YQ, Yang Y, Fei Z, Yuan H, Fish T, Thannhauser TW, et al. Proteomic analysis of chromoplasts from six crop species reveals insights into chromoplast function and development. J Exp Bot. 2013; 64: 949-961. doi: 10.1093/jxb/ers375 PMID: 23314817
15. Zeng Y, Pan Z, Wang L, Ding Y, Xu Q, Xiao S, et al. Phosphoproteomic analysis of chromoplasts from sweet orange during fruit ripening. Physiol Plant 2014; 150: 252-270. doi: 10.1111/ppl.12080 PMID: 23786612
16. Akerstrom B, Flower DR, Salier JP. Lipocalins: Unity in diversity. Biochim Biophys Acta. 2006; 163: 895-915.
17. Grzyb J, Latowski D, Strzalka K. Lipocalins-A family portrait. Journal of Plant Physiology 2006; 163: 895-915. PMID: 16504339
18. Frenette Charron JB, Breton G, Badawi M, Sarhan F. Molecular and structural analyses of a novel temperature stress-induced lipocalin from wheat and Arabidopsis. FEBS Lett. 2002; 517: 129-132. PMID: 12062422
19. Frenette Charron JB, Ouellet F, Pelletier M, Danyluk J, Chauve C, Sarhan F. Identification, expression, and evolutionary analyses of plant lipocalins. Plant Physiol. 2005; 139: 2017-2028. PMID: 16306142
20. Giovannoni J. Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mol Biol. 2001; 52: 725-749. PMID: 11337414
21. Adams-Phillips L, Barry C, Giovannoni J. Signal transduction systems regulating fruit ripening. Trends Plant Sci. 2004; 9: 331-338. PMID: 15231278
22. Mueller LA, Tanksley SD, Giovannoni JJ, van Eck J, Stack S, Choi D, et al. The tomato sequencing project, the first cornerstone of the international Solanaceae project (SOL). Comp Funct Genomics 2005; 6: 153-158. doi: 10.1002/cfg.468 PMID: 18629226
23. Tomato Genome Consortium. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 2012; 485: 635-641. doi: 10.1038/nature11119 PMID: 22660326
24. Kalhau S, Aspinall S, Gray JC, Bock R. Sequence of the tomato chloroplast DNA and evolutionary comparison of Solanaceous plastid genomes. J Mol Evol. 2006; 63: 194-207. PMID: 16830097
25. Aoki K, Yano K, Suzuki A, Kawamura S, Sakurai N, Suda K, et al. Large-scale analysis of full-length cDNAs from the tomato (Solanum lycopersicum) cultivar Micro-Tom, a reference system for the Solanaceae genomics. BMC Genomics 2010; 11: 210-226. doi: 10.1186/1471-2164-11-210 PMID: 20350329
26. Karlova R, Rosin FM, Busscher-Lange J, Parapunova V, Do PT, Fernie AR, et al. Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 2011; 23: 923-941. doi: 10.1105/tpc.110.081273 PMID: 21398570
27. Matas AJ, Yeats TH, Buda GJ, Zheng Y, Chatterjee S, Tohge T, et al. Tissue-And cell-Type specific transcriptome profiling of expanding tomato fruit provides insights into metabolic and regulatory specialization and cuticle formation. Plant Cell 2011; 23: 3893-3910. doi: 10.1105/tpc.111.091173 PMID: 22045915
28. Kahlau S, Bock R. Plastid transcriptomics and translatomics of tomato fruit development and chloroplast-To-chromoplast differentiation: Chromoplast gene expression largely serves the production of a single protein. Plant Cell 2008; 20: 856-874. doi: 10.1105/tpc.107.055202 PMID: 18441214
29. Mintz-Oron S, Mandel T, Rogachev I, Feldberg L, Lotan O, Yativ M, et al. Gene expression and metabolism in tomato fruit surface tissues. Plant Physiol. 2008; 147: 823-851. doi: 10.1104/pp.108.116004 PMID: 18441227
30. Vogel JT, Tieman DM, Sims CA, Odabasi A, Clark DG, Klee HJ. Carotenoid content impacts flavor acceptability in tomato (Solanum lycopersicum). J Sci Food Agric. 2010; 90: 2233-2240. doi: 10.1002/jsfa.4076 PMID: 20661902
31. Adato A, Mandel T, Mintz-Oron S, Venger I, Levy D, Yativ M, et al. Fruit-surface flavonoid accumulation in tomato is controlled by a SlMYB12-regulated transcriptional network. PLoS Genet. 2009; 5(12); e1000777. doi: 10.1371/journal.pgen.1000777 PMID: 20019811
32. Iijima Y, Nakamura Y, Ogata Y, Tanaka K, Sakurai N, Suda K, et al. Metabolite annotations based on the integration of mass spectral information. Plant J. 2008; 54: 949-962. doi: 10.1111/j.1365-313X. 2008.03434.x PMID: 18266924
33. Martí E, Gisbert C, Bishop GJ, Dixon MS, García-Martínez JL. Genetic and physiological characterization of tomato cv. Micro-Tom. J Exp Bot. 2006; 57: 2037-2047. PMID: 16687436
34. Tetlow IJ, Bowsher CG, Emes MJ. Biochemical properties and enzymic capacities of chromoplasts isolated from wild buttercup (Ranunculus acris L.). Plant Science 2003; 165: 383-394.
35. Lord JM, Kagawa T, Moore TS, Beevers H. Endoplasmic reticulum as the site of lecithin formation in castor bean endosperm. J Cell Biol. 1973; 57: 659-667. PMID: 4144630
36. Ray PM, Shininger TL, Ray MM. Isolation of β-Glucan synthetase particles from plant cells and identification with Golgi membranes. Proc Natl Acad Sci U S A. 1969; 64: 605-612. PMID: 16591795
37. Fujiwara M, Hamada S, Hiratsuka M, Fukao Y, Kawasaki T, Shimamoto K Proteome analysis of detergent-resistant membranes (DRMs) associated with OsRac1-mediated innate immunity in rice. Plant Cell Physiol. 2009; 50: 1191-1200. doi: 10.1093/pcp/pcp077 PMID: 19502382
38. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999; 20: 3551-3567. PMID: 10612281
39. Poole RL. The TAIR database. Methods Mol Biol. 2007; 406: 179-212. PMID: 18287693
40. Thimm O, Blaesing O, Gibon Y, Nagel A, Meyer S, Krüger P, et al. MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 2004; 37(6): 914-939. PMID: 14996223
41. Maere S, Heymans K, Kuiper M. BiNGO: A Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics. 2005; 21: 3448-3449. PMID: 15972284
42. Kato M, Ikoma Y, Matsumoto H, Sugiura M, Hyodo H, Yano M. Accumulation of carotenoids and expression of carotenoid biosynthetic genes during maturation in citrus fruit. Plant Physiol. 2004; 134: 824-837. PMID: 14739348
43. Egea I, Barsan C, Bian W, Purgatto E, Latché A, Li Z, et al. Chromoplast differentiation: Current status and perspectives. Plant Cell Physiol. 2010; 51: 1601-1611. doi: 10.1093/pcp/pcq136 PMID: 20801922
44. Kleffmann T, Hirsch-Hoffmann M, Gruissem W, Baginsky S. Proteome dynamics during plastid differentiation in rice. Plant Cell Physiol. 2006; 47: 432-436.
45. Vishnevetsky M, Ovadis M, Zuker A, Vainstein A. Molecular mechanisms underlying carotenogenesis in the chromoplast: Multilevel regulation of carotenoid-Associated genes. Plant J. 1999; 20: 423-431. PMID: 10607295
46. Vishnevetsky M, Ovadis M, Itzhaki H, Levy M, Libal-Weksler Y, Adam Z, et al. Molecular cloning of a carotenoid-Associated protein from Cucumis sativus corollas: Homologous genes involved in carotenoid sequestration in chromoplasts. Plant J. 1996; 10: 1111-1118. PMID: 9011091
47. Kilambi HV, Kumar R, Sharma R, Sreelakshmi Y. Chromoplast-specific carotenoid-Associated protein appears to be important for enhanced accumulation of carotenoids in hp1 tomato fruits. Plant Physiol. 2013; 161: 2085-2101. doi: 10.1104/pp.112.212191 PMID: 23400702
48. Motohashi R, Yamazaki T, Myouga F, Ito T, Ito K, Satou M, et al. Chloroplast ribosome release factor 1 (AtcpRF1) is essential for chloroplast development. Plant Mol Biol. 2007; 64: 481-497. PMID: 17450416
49. Blanke MM, Lenz F. Fruit photosynthesis. Plant Cell Environ. 1989; 12: 31-46.
50. Carrara S, Pardossi A, Soldatini GF, Tognoni F, Guide L. Photosynthetic activity of ripening tomato fruit. Photosynthetica 2001; 39: 75-78.
51. Borisjuk L, Rolletschek H. The oxygen status of the developing seed. New Phytol. 2009; 182: 17-30. doi: 10.1111/j.1469-8137.2008.02752.x PMID: 19207684
52. Kalachanis D, Manetas Y. Analysis of fast chlorophyll fluorescence rise (O-K-J-I-P) curves in green fruits indicates electron flow limitations at the donor side of PSII and the acceptor sides of both photosystems. Physiol Plant 2010; 139: 313-323. doi: 10.1111/j.1399-3054.2010.01362.x PMID: 20149129
53. Ruuska SA, Schwender J, Ohlrogge JB. The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes. Plant Physiol. 2004; 136: 2700-2709. PMID: 15347783
54. Camara B, Hugueney P, Bouvier F, Kuntz M, Monéger R. Biochemistry and molecular biology of chromoplast development. Int. Rev. Cytol. 1995; 163: 175-247. PMID: 8522420
55. Vasquez-Caicedo AL, Heller A, Neidhart S, Carle R. Chromoplast morphology and beta-carotene accumulation during postharvest ripening of Mango Cv. 'Tommy Atkins'. J Agric Food Chem. 2006; 54: 5769-5776. PMID: 16881676
56. Charron J-BF, Ouellet F, Houde M, Sarhan F. The plant apolipoprotein D ortholog protects Arabidopsis against oxidative stress. BMC Plant Biology 2008; 8: 86 doi: 10.1186/1471-2229-8-86 PMID: 18671872
57. Martí MC, Camejo D, Olmos E, Sandalio LM, Fernández-García N, Jiménez A, et al. Characterisation and changes in the antioxidant system of chloroplasts and chromoplasts isolated from green and mature pepper fruits. Plant Biol (Stuttg). 2009; 11: 613-624.
58. Livne A, Gepstein S. Abundance of the major chloroplast polypeptides during development and ripening of tomato fruits: An immunological study. Plant Physiol. 1988; 87: 239-243. PMID: 16666110
59. Gady AL, Vriezen WH, Van de Wal MH, Huang P, Bovy AG, Visser RG, et al. Induced point mutations in the phytoene synthase 1 gene cause differences in carotenoid content during tomato fruit ripening. Mol Breeding 2012; 29: 801-812.
60. Fray GR, Grierson D. Identification and genetic analysis of normal and mutant phytoene synthase genes of tomato by sequencing, complementation and co-suppression. Plant Mol Biol. 1993; 22: 589-602. PMID: 8343597
61. Hunt GM, Baker EA. Phenolic constituents of tomato fruit cuticles. Phytochemistry 1980; 19: 1415-1419.
62. Leitner-Dagan Y, Ovadis M, Shklarman E, Elad Y, Rav David D, Vainstein A. Expression and functional analyses of the plastid lipid-Associated protein CHRC suggest its role in chromoplastogenesis and stress. Plant Physiol. 2006; 142: 233-244. PMID: 16815957
63. Chi WT, Fung RW, Liu HC, Hsu CC, Charng YY. Temperature-induced lipocalin is required for basal and acquired thermotolerance in Arabidopsis. Plant Cell Environ. 2009; 32: 917-927. doi: 10.1111/j. 1365-3040.2009.01972.x PMID: 19302169
64. Flower DR. The lipocalin protein family: Structure and function. Biochem J. 1996; 318: 1-14. PMID: 8761444
65. Jones AM, Bennett MH, Mansfield JW, Grant M. Analysis of the defence phosphoproteome of Arabidopsis thaliana using differential mass tagging. Proteomics 2006; 14: 4155-4165.
66. Simkin AJ, Gaffé J, Alcaraz JP, Carde JP, Bramley PM, Fraser PD, et al. Fibrillin influence on plastid ultrastructure and pigment content in tomato fruit. Phytochemistry. 2007; 68: 1545-1556. PMID: 17466343
67. You J, Fitzgerald A, Cozzi PJ, Zhao Z, Graham P, Russell PJ, et al. Post-Translation modification of proteins in tears. Electrophoresis 2010; 31: 1853-1861. doi: 10.1002/elps.200900755 PMID: 20506419