Chromoplast-specific carotenoid-associated protein appears to be important for enhanced accumulation of carotenoids in hp1 tomato fruits

Plant Physiology

Volumn 161, Issue 4, 2013, Pages 2085-2101

  Kilambi, Himabindu Vasuki ^a   Kumar, Rakesh ^a   Sharma, Rameshwar ^a   Sreelakshmi, Yellamaraju ^a  

^a UNIVERSITY OF HYDERABAD   (India)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84875698944     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.212191     Document Type: Article

References (73)

1. Austin JR II, Frost E, Vidi PA, Kessler F, Staehelin LA (2006) Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18: 1693-1703.
2. Azari R, Tadmor Y, Meir A, Reuveni M, Evenor D, Nahon S, Shlomo H, Chen L, Levin I (2010) Light signaling genes and their manipulation towards modulation of phytonutrient content in tomato fruits. Biotechnol Adv 28: 108-118.
3. Barba AIO, Hurtado MC, Mata MCS, Ruiz VF, de Tejada MLS (2006) Application of a UV-vis detection-HPLC method for a rapid determination of lycopene and b-carotene in vegetables. Food Chem 95: 328-336.
4. Barsan C, Sanchez-Bel P, Rombaldi C, Egea I, Rossignol M, Kuntz M, Zouine M, Latché A, Bouzayen M, Pech JC (2010) Characteristics of the tomato chromoplast revealed by proteomic analysis. J Exp Bot 61: 2413-2431.
5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57: 289-300.
6. Bernhardt A, Lechner E, Hano P, Schade V, Dieterle M, Anders M, Dubin MJ, Benvenuto G, Bowler C, Genschik P, et al (2006) CUL4 associates with DDB1 and DET1 and its downregulation affects diverse aspects of development in Arabidopsis thaliana. Plant J 47: 591-603.
7. Bernhardt A, Mooney S, Hellmann H (2010) Arabidopsis DDB1a and DDB1b are critical for embryo development. Planta 232: 555-566.
8. Besagni C, Piller LE, Brehelin C (2011) Preparation of plastoglobules from Arabidopsis plastids for proteomic analysis and other studies. Methods Mol Biol 775: 223-239.
9. Bian W, Barsan C, Egea I, Purgatto E, Chervin C, Zouine M, Latché A, Bouzayen M, Pech JC (2011) Metabolic and molecular events occurring during chromoplast biogenesis. J Bot 2011: 1-13.
10. Bianco L, Lopez L, Scalone AG, Di Carli M, Desiderio A, Benvenuto E, Perrotta G (2009) Strawberry proteome characterization and its regulation during fruit ripening and in different genotypes. J Proteomics 72: 586-607.
11. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
12. Bréhélin C, Kessler F (2008) The plastoglobule: a bag full of lipid biochemistry tricks. Photochem Photobiol 84: 1388-1394.
13. Caraux G, Pinloche S (2005) PermutMatrix: a graphical environment to arrange gene expression profiles in optimal linear order. Bioinformatics 21: 1280-1281.
14. Carrari F, Fernie AR (2006) Metabolic regulation underlying tomato fruit development. J Exp Bot 57: 1883-1897.
15. Carvalho RF, Aidar ST, Azevedo RA, Dodd IC, Peres LE (2011) Enhanced transpiration rate in the high pigment 1 tomato mutant and its physiological significance. Plant Biol (Stuttg) 13: 546-550.
16. Chen H, Huang X, Gusmaroli G, Terzaghi W, Lau OS, Yanagawa Y, Zhang Y, Li J, Lee JH, Zhu D, et al (2010) Arabidopsis CULLIN4- damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1-SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time. Plant Cell 22: 108-123.
17. Cookson PJ, Kiano JW, Shipton CA, Fraser PD, Romer S, Schuch W, Bramley PM, Pyke KA (2003) Increases in cell elongation, plastid compartment size and phytoene synthase activity underlie the phenotype of the high pigment-1 mutant of tomato. Planta 217: 896-903.
18. Davuluri GR, van Tuinen A, Fraser PD, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J, et al (2005) Fruitspecific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat Biotechnol 23: 890-895.
19. Deruère J, Bouvier F, Steppuhn J, Klein A, Camara B, Kuntz M (1994) Structure and expression of two plant genes encoding chromoplastspecific proteins: occurrence of partially spliced transcripts. Biochem Biophys Res Commun 199: 1144-1150.
20. Egea I, Bian W, Barsan C, Jauneau A, Pech JC, Latché A, Li Z, Chervin C (2011) Chloroplast to chromoplast transition in tomato fruit: spectral confocal microscopy analyses of carotenoids and chlorophylls in isolated plastids and time-lapse recording on intact live tissue. Ann Bot (Lond) 108: 291-297.
21. Enfissi EM, Barneche F, Ahmed I, Lichtlé C, Gerrish C, McQuinn RP, Giovannoni JJ, Lopez-Juez E, Bowler C, Bramley PM, et al (2010) Integrative transcript and metabolite analysis of nutritionally enhanced DE-ETIOLATED1 downregulated tomato fruit. Plant Cell 22: 1190-1215.
22. Eravci M, Mansmann U, Broedel O, Weist S, Buetow S, Wittke J, Brunkau C, Hummel M, Eravci S, Baumgartner A (2009) Strategies for a reliable biostatistical analysis of differentially expressed spots from twodimensional electrophoresis gels. J Proteome Res 8: 2601-2607.
23. Faurobert M, Mihr C, Bertin N, Pawlowski T, Negroni L, Sommerer N, Causse M (2007) Major proteome variations associated with cherry tomato pericarp development and ripening. Plant Physiol 143: 1327-1346.
24. Fernie AR, Stitt M (2012) On the discordance of metabolomics with proteomics and transcriptomics: coping with increasing complexity in logic, chemistry, and network interactions scientific correspondence. Plant Physiol 158: 1139-1145.
25. Fraser PD, Enfissi EM, Halket JM, Truesdale MR, Yu D, Gerrish C, Bramley PM (2007) Manipulation of phytoene levels in tomato fruit: effects on isoprenoids, plastids, and intermediary metabolism. Plant Cell 19: 3194-3211.
26. Frenette Charron JB, Breton G, Badawi M, Sarhan F (2002) Molecular and structural analyses of a novel temperature stress-induced lipocalin from wheat and Arabidopsis. FEBS Lett 517: 129-132.
27. Galpaz N, Wang Q, Menda N, Zamir D, Hirschberg J (2008) Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J 53: 717-730.
28. Giuliano G, Bartley GE, Scolnik PA (1993) Regulation of carotenoid biosynthesis during tomato development. Plant Cell 5: 379-387.
29. Goldring JP, Ravaioli L (1996) Solubilization of protein-dye complexes on nitrocellulose to quantify proteins spectrophotometrically. Anal Biochem 242: 197-201.
30. Harris WM, Spurr AR (1969) Chromoplasts of tomato fruits. II. The red tomato. Am J Bot 56: 380-389.
31. Hieber AD, Bugos RC, Yamamoto HY (2000) Plant lipocalins: violaxanthin de-epoxidase and zeaxanthin epoxidase. Biochim Biophys Acta 1482: 84-91.
32. Isaacson T, Damasceno CM, Saravanan RS, He Y, Catalá C, Saladié M, Rose JK (2006) Sample extraction techniques for enhanced proteomic analysis of plant tissues. Nat Protoc 1: 769-774.
33. Jones CM (2000) Evaluation of carotenoids and anthocyanins in high pigment, processing, heirloom and anthocyanin fruit tomatoes. MS thesis. Oregon State University, Corvallis
34. Kendrick RE, Kerckhoffs LH, van Tuinen A, Koornneef M (1997) Photomorphogenic mutants of tomato. Plant Cell Environ 20: 746-751.
35. Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45: 41-59.
36. Kolotilin I, Koltai H, Tadmor Y, Bar-Or C, Reuveni M, Meir A, Nahon S, Shlomo H, Chen L, Levin I (2007) Transcriptional profiling of high pigment-2dg tomato mutant links early fruit plastid biogenesis with its overproduction of phytonutrients. Plant Physiol 145: 389-401.
37. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
38. Lavi N, Tadmor Y, Meir A, Bechar A, Oren-Shamir M, Ovadia R, Reuveni M, Nahon S, Shlomo H, Chen L, et al (2009) Characterization of the intense pigment tomato genotype emphasizing targeted fruit metabolites and chloroplast biogenesis. J Agric Food Chem 57: 4818-4826.
39. Leitner-Dagan Y, Ovadis M, Shklarman E, Elad Y, Rav David D, Vainstein A (2006) Expression and functional analyses of the plastid lipid-associated protein CHRC suggest its role in chromoplastogenesis and stress. Plant Physiol 142: 233-244.
40. Lenucci MS, Serrone L, De Caroli M, Fraser PD, Bramley PM, Piro G, Dalessandro G (2012) Isoprenoid, lipid, and protein contents in intact plastids isolated from mesocarp cells of traditional and high-pigment tomato cultivars at different ripening stages. J Agric Food Chem 60: 1764-1775.
41. Levin I, Frankel P, Gilboa N, Tanny S, Lalazar A (2003) The tomato dark green mutation is a novel allele of the tomato homolog of the DEETIOLATED1 gene. Theor Appl Genet 106: 454-460.
42. Li L, Yang Y, Xu Q, Owsiany K, Welsch R, Chitchumroonchokchai C, Lu S, Van Eck J, Deng XX, Failla M, et al (2012) The Or gene enhances carotenoid accumulation and stability during post-harvest storage of potato tubers. Mol Plant 5: 339-352.
43. Lieberman M, Segev O, Gilboa N, Lalazar A, Levin I (2004) The tomato homolog of the gene encoding UV-damaged DNA binding protein 1 (DDB1) underlined as the gene that causes the high pigment-1 mutant phenotype. Theor Appl Genet 108: 1574-1581.
44. Liu Y, Roof S, Ye Z, Barry C, van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101: 9897-9902.
45. Lu S, Van Eck J, Zhou X, Lopez AB, O'Halloran DM, Cosman KM, Conlin BJ, Paolillo DJ, Garvin DF, Vrebalov J, et al (2006) The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of b-carotene accumulation. Plant Cell 18: 3594-3605.
46. Lundquist PK, Poliakov A, Bhuiyan NH, Zybailov B, Sun Q, van Wijk KJ (2012) The functional network of the Arabidopsis plastoglobule proteome based on quantitative proteomics and genome-wide coexpression analysis. Plant Physiol 158: 1172-1192.
47. Manaa A, Ben Ahmed H, Valot B, Bouchet JP, Aschi-Smiti S, Causse M, Faurobert M (2011) Salt and genotype impact on plant physiology and root proteome variations in tomato. J Exp Bot 62: 2797-2813.
48. Mounet F, Moing A, Garcia V, Petit J, Maucourt M, Deborde C, Bernillon S, Le Gall G, Colquhoun I, Defernez M, et al (2009) Gene and metabolite regulatory network analysis of early developing fruit tissues highlights new candidate genes for the control of tomato fruit composition and development. Plant Physiol 149: 1505-1528.
49. Mustilli AC, Fenzi F, Ciliento R, Alfano F, Bowler C (1999) Phenotype of the tomato high pigment-2 mutant is caused by a mutation in the tomato homolog of DEETIOLATED1. Plant Cell 11: 145-157.
50. Osorio S, Alba R, Damasceno CM, Lopez-Casado G, Lohse M, Zanor MI, Tohge T, Usadel B, Rose JK, Fei Z, et al (2011) Systems biology of tomato fruit development: combined transcript, protein, and metabolite analysis of tomato transcription factor (nor, rin) and ethylene receptor (Nr) mutants reveals novel regulatory interactions. Plant Physiol 157: 405-425.
51. Pozueta-Romero J, Rafia F, Houlné G, Cheniclet C, Carde JP, Schantz ML, Schantz R (1997) A ubiquitous plant housekeeping gene, PAP, encodes a major protein component of bell pepper chromoplasts. Plant Physiol 115: 1185-1194.
52. Qin G, Wang Y, Cao B, Wang W, Tian S (2012) Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening. Plant J 70: 243-255.
53. Rocco M, D'Ambrosio C, Arena S, Faurobert M, Scaloni A, Marra M (2006) Proteomic analysis of tomato fruits from two ecotypes during ripening. Proteomics 6: 3781-3791.
54. Rohrmann J, Tohge T, Alba R, Osorio S, Caldana C, McQuinn R, Arvidsson S, van der Merwe MJ, Riaño-Pachón DM, Mueller-Roeber B, et al (2011) Combined transcription factor profiling, microarray analysis and metabolite profiling reveals the transcriptional control of metabolic shifts occurring during tomato fruit development. Plant J 68: 999-1013.
55. Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Güldener U, Mannhaupt G, Münsterkötter M, et al (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32: 5539-5545.
56. Saito K, Hirai MY, Yonekura-Sakakibara K (2008) Decoding genes with coexpression networks and metabolomics: 'majority report by precogs.' Trends Plant Sci 13: 36-43.
57. Santisree P, Nongmaithem S, Vasuki H, Sreelakshmi Y, Ivanchenko MG, Sharma R (2011) Tomato root penetration in soil requires a coaction between ethylene and auxin signaling. Plant Physiol 156: 1424-1438.
58. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1: 2856-2860.
59. Siddique MA, Grossmann J, Gruissem W, Baginsky S (2006) Proteome analysis of bell pepper (Capsicum annuum L.) chromoplasts. Plant Cell Physiol 47: 1663-1673.
60. Simkin AJ, Gaffé J, Alcaraz JP, Carde JP, Bramley PM, Fraser PD, Kuntz M (2007) Fibrillin influence on plastid ultrastructure and pigment content in tomato fruit. Phytochemistry 68: 1545-1556.
61. Smirra I, Halevy AH, Vainstein A (1993) Isolation and characterization of a chromoplast-specific carotenoid-associated protein from Cucumis sativus corollas. Plant Physiol 102: 491-496.
62. Speirs J, Lee E, Holt K, Yong-Duk K, Scott NS, Loveys B, Schuch W(1998) Genetic manipulation of alcohol dehydrogenase levels in ripening tomato fruit affects the balance of some flavor aldehydes and alcohols. Plant Physiol 117: 1047-1058.
63. Sreelakshmi Y (2000) Regulation and characterization of tomato phenylalanine ammonia-lyase(s). PhD thesis. University of Hyderabad, Hyderabad, India
64. Srinivas A, Behera RK, Kagawa T, Wada M, Sharma R (2004) High pigment1 mutation negatively regulates phototropic signal transduction in tomato seedlings. Plant Physiol 134: 790-800.
65. Stigliani AL, Giorio G, D'Ambrosio C (2011) Characterization of P450 carotenoid beta- and epsilon-hydroxylases of tomato and transcriptional regulation of xanthophyll biosynthesis in root, leaf, petal and fruit. Plant Cell Physiol 52: 851-865.
66. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350-4354.
67. Vainstein A, Halevy AH, Smirra I, Vishnevetsky M (1994) Chromoplast biogenesis in Cucumis sativus corollas (rapid effect of gibberellin A3 on the accumulation of a chromoplast-specific carotenoid-associated protein). Plant Physiol 104: 321-326.
68. Vishnevetsky M, Ovadis M, Vainstein A (1999) Carotenoid sequestration in plants: the role of carotenoid-associated proteins. Trends Plant Sci 4: 232-235.
69. Wang S, Liu J, Feng Y, Niu X, Giovannoni J, Liu Y (2008) Altered plastid levels and potential for improved fruit nutrient content by downregulation of the tomato DDB1-interacting protein CUL4. Plant J 55: 89-103.
70. Ytterberg AJ, Peltier JB, van Wijk KJ (2006) Protein profiling of plastoglobules in chloroplasts and chromoplasts: a surprising site for differential accumulation of metabolic enzymes. Plant Physiol 140: 984-997.
71. Zeng Y, Pan Z, Ding Y, Zhu A, Cao H, Xu Q, Deng X (2011) A proteomic analysis of the chromoplasts isolated from sweet orange fruits [Citrus sinensis (L.) Osbeck]. J Exp Bot 62: 5297-5309.
72. Zhang J, Ma H, Feng J, Zeng L, Wang Z, Chen S (2008) Grape berry plasma membrane proteome analysis and its differential expression during ripening. J Exp Bot 59: 2979-2990.
73. Zhou X, Van Eck J, Li L (2008) Use of the cauliflower Or gene for improving crop nutritional quality. Biotechnol Annu Rev 14: 171-190.