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The Proteome of Fruit Peroxisomes: Sweet Pepper (Capsicum annuum L.) as a Model

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Part of the Subcellular Biochemistry book series (SCBI, volume 89)

Abstract

Despite of their economical and nutritional interest, the biology of fruits is still little studied in comparison with reports of other plant organs such as leaves and roots. Accordingly, research at subcellular and molecular levels is necessary not only to understand the physiology of fruits, but also to improve crop qualities. Efforts addressed to gain knowledge of the peroxisome proteome and how it interacts with the overall metabolism of fruits will provide tools to be used in breeding strategies of agricultural species with added value. In this work, special attention will be paid to peroxisomal proteins involved in the metabolism of reactive oxygen species (ROS) due to the relevant role of these compounds at fruit ripening. The proteome of peroxisomes purified from sweet pepper (Capsicum annuum L.) fruit is reported, where an iron-superoxide dismutase (Fe-SOD) was localized in these organelles, besides other antioxidant enzymes such as catalase and a Mn-SOD, as well as enzymes involved in the metabolism of carbohydrates, malate, lipids and fatty acids, amino acids, the glyoxylate cycle and in the potential organelles’ movements.

Keywords

Catalase Olive fruits Pepper fruits Reactive oxygen species (ROS) Ripening Superoxide dismutase 

Abbreviations

ACO

Aconitase

ALDH

Aldehyde dehydrogenase

FDH

Formate dehydrogenase

GDC

Glycine decarboxylase

MALDI-TOF/TOF

Matrix-assisted laser desorption/ionization-time of flight

NO

Nitric oxide

PGK

Phosphoglycerate kinase

RNS

Reactive nitrogen species

ROS

Reactive oxygen species

SOD

Superoxide dismutase

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Notes

Acknowledgements

This work was supported by the ERDF-cofinanced grants AGL2011-26044 and AGL2015-65104-P from the Ministry of Economy and Competitiveness, Spain.

References

  1. Álvarez de Morales P, Jiménez A, Chaki M, Bonilla-Valverde D, Campos MJ, del Río LA, Sevilla F, Corpas FJ, Palma JM (2011) Proteomics of pepper (Capsicum annuum L.) fruits during ripening. In: XXIV Scandinavian Plant Physiology Society (SPPS) Congress, Stavanger, Norway, Abstract BookGoogle Scholar
  2. Ast J, Stiebler AC, Freitag J, Bölker M (2013) Dual targeting of peroxisomal proteins. Front Physiol/Integr Physiol 4:297Google Scholar
  3. Baker A, Graham IA, Holdsworth M, Smith SM, Theodoulou FL (2006) Chewing the fat: β-oxidation in signalling and development. Trends Plant Sci 11:124–132CrossRefGoogle Scholar
  4. Barsan C, Sanchez-Bel P, Rombaldi C, Egea I, Rossignol M, Kuntz M, Mohamed Zouine M, Alain Latché A, Mondher Bouzayen M, Pech J-C (2010) Characteristics of the tomato chromoplast revealed by proteomic analysis. J Exp Bot 61:2413–2431CrossRefGoogle Scholar
  5. Barsan C, Zouine M, Maza E, Bian W, Egea I, Rossignol M, Bouyssie D, Pichereaux C, Purgatto E, Bouzayen M, Latché A, Pech J-C (2012) 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 160:708–725CrossRefPubMedGoogle Scholar
  6. Barsan C, Kuntz M, Pech JC (2017) Isolation of chromoplasts and suborganellar compartments from tomato and bell pepper fruit. Methods Mol Biol 1511:61–71CrossRefGoogle Scholar
  7. Bauer S, Morris MT (2017) Glycosome biogenesis in Trypanosomes and the de novo dilemma. PLoS Negl Trop Dis 11:e0005333CrossRefPubMedGoogle Scholar
  8. Bianchetti RE, Cruz AB, Oliveira BS, Demarco D, Purgatto E, Pereira Peres LEP, Rossi M, Freschi L (2017) Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits. Sci Reports 7:7822CrossRefGoogle Scholar
  9. Blattner J, Helfert S, Michels P, Clayton C (1998) Compartmentation of phosphoglycerate kinase in Trypanosoma brucei plays a critical role in parasite energy metabolism. Proc Natl Acad Sci USA 95:11596–11600CrossRefGoogle Scholar
  10. Bowler MW (2013) Conformational dynamics in phosphoglycerate kinase, an open and shut case? FEBS Lett 587:1878–1883CrossRefPubMedGoogle Scholar
  11. Bruley C, Dupierris V, Salvi D, Rolland N, Ferro M (2012) AT_CHLORO: a chloroplast protein database dedicated to sub-plastidial localization. Front Plant Sci 3:205CrossRefPubMedGoogle Scholar
  12. Bussell JD, Behrens C, Ecke W, Eubel H (2013) Arabidopsis peroxisome proteomics. Front Plant Sci 4:101Google Scholar
  13. Camejo D, Jiménez A, Palma JM, Sevilla F (2015) Proteomic identification of mitochondrial carbonylated proteins in two maturation stages of pepper fruits. Proteomics 15:2634–2642CrossRefPubMedGoogle Scholar
  14. Chaki M, Álvarez de Morales P, Ruiz C, Begara-Morales JC, Barroso JB, Corpas FJ, Palma JM (2015) Ripening of pepper (Capsicum annuum) fruit is characterized by an enhancement of protein tyrosine nitration. Ann Bot 116:637–647CrossRefPubMedGoogle Scholar
  15. Corpas FJ, Barroso JB (2014) Peroxynitrite (ONOO-) is endogenously produced in Arabidopsis peroxisomes and is overproduced under cadmium stress. Ann Bot 113:87–96CrossRefPubMedGoogle Scholar
  16. Corpas FJ, Leterrier M, Begara-Morales JC, Valderrama R, Chaki M, López-Jaramillo J, Luque F, Palma JM, Padilla MN, Sánchez-Calvo B, Mata-Pérez C, Barroso JB (2013) Inhibition of peroxisomal hydroxypyruvate reductase (HPR1) by tyrosine nitration. Biochim Biophys Acta 1830:4981–4989CrossRefPubMedGoogle Scholar
  17. Corpas FJ, Barroso JB, Palma JM, Rodríguez-Ruiz M (2017) Plant peroxisomes: a nitro-oxidative cocktail. Redox Biol 11:535–542CrossRefPubMedGoogle Scholar
  18. Corpas FJ, Freschi L, Rodríguez-Ruiz M, Mioto PT, González-Gordo S, Palma JM (2018) Nitro-oxidative metabolism during fruit ripening. J Exp Bot.  https://doi.org/10.1093/jxb/erx453CrossRefPubMedGoogle Scholar
  19. de la Torre F, Cañas RA, Pascual MB, Ávila C, Cánovas FM (2014) Plastidic aspartate aminotransferases and the biosynthesis of essential amino acids in plants. J Exp Bot 65:5527–5534CrossRefPubMedGoogle Scholar
  20. Degu A, Hatew B, Nunes-Nesi A, Shlizerman L, Zur N, Katz E, Fernie AR, Blumwald E, Sadka A (2011) Inhibition of aconitase in citrus fruit callus results in a metabolic shift towards amino acid biosynthesis. Planta 234:501–513CrossRefGoogle Scholar
  21. del Río LA, López-Huertas E (2016) ROS generation in peroxisomes and its role in cell signaling. Plant Cell Physiol 57:1364–1376Google Scholar
  22. del Río LA, Sandalio LM, Altomare DA, Zilinskas BA (2003) Mitochondrial and peroxisomal manganese superoxide dismutase: differential expression during leaf senescence. J Exp Bot 54:923–933CrossRefGoogle Scholar
  23. Droillard MJ, Paulin A (1990) Isozymes of superoxide dismutase in mitocondria and peroxisomes isolated from petals of carnation (Dianthus caryophyllus) during senescence. Plant Physiol 94:1187–1192CrossRefPubMedGoogle Scholar
  24. du Choi S, Kim NH, Hwang BK (2014) Pepper mitochondrial FORMATE DEHYDROGENASE1 regulates cell death and defense responses against bacterial pathogens. Plant Physiol 166:1298–1311CrossRefPubMedGoogle Scholar
  25. Du L, Song J, Forney C, Palmer LC, Fillmore S, Qi Z (2016) Proteome changes in banana fruit peel tissue in response to ethylene and high-temperature treatments. Hortic Res 3:16012CrossRefPubMedGoogle Scholar
  26. Eubel H, Meyer EH, Taylor NL, Bussell JD, O’Toole N, Heazlewood JL, Castleden I, Small ID, Smith SM, Millar AH (2008) Novel proteins, putative membrane transporters, and an integrated metabolic network are revealed by quantitative proteomic analysis of Arabidopsis cell culture peroxisomes. Plant Physiol 148:1809–1829CrossRefPubMedGoogle Scholar
  27. Ferro M, Brugière S, Salvi D, Seigneurin-Berny D, Court M, Moyet L, Ramus C, Miras S, Mellal M, Le Gall S, Kieffer-Jaquinod S, Bruley C, Garin J, Joyard J, Masselon C, Rolland N (2010) AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 9:1063–1084CrossRefPubMedGoogle Scholar
  28. Fray RG, Grierson D (1993) Molecular genetics of tomato fruit ripening. Trends Genet 9:438–443CrossRefPubMedGoogle Scholar
  29. Freitag J, Ast J, Bölker M (2012) Cryptic peroxisomal targeting via alternative splicing and stop codon read-through in fungi. Nature 485:522–525CrossRefGoogle Scholar
  30. Fujiwara T, Hori K, Ozaki K, Yokota Y, Mitsuya S, Ichiyanagi T, Hattori T, Takabe T (2008) Enzymatic characterization of peroxisomal and cytosolic betaine aldehyde dehydrogenases in barley. Physiol Plant 134:22–30CrossRefGoogle Scholar
  31. Fukao Y, Hayashi M, Nishimura M (2002) Proteomic analysis of leaf peroxisomal proteins in greening cotyledons of Arabidopsis thaliana. Plant Cell Physiol 43:689–696CrossRefGoogle Scholar
  32. Ganguly A, Dixit R (2013) Mechanisms for regulation of plant kinesins. Current Op Plant Biol 16:704–709CrossRefGoogle Scholar
  33. Gerhardt B (1992) Fatty-acid degradation in plants. Prog Lipid Res 31:417–446CrossRefGoogle Scholar
  34. Gerhardt B, Fischer K, Balkenhohl TJ, Pohnert G, Kuhn H, Wasternack C, Feussner I (2005) Lipoxygenase-mediated metabolism of storage lipids in germinating sunflower cotyledons and beta-oxidation of (9Z,11E,13S)-13-hydroxy-octadeca-9,11-dienoic acid by the cotyledonary glyoxysomes. Planta 220:919–930CrossRefGoogle Scholar
  35. Haanstra JR, González-Marcano EB, Gualdrón-López M, Michels PAM (2016) Biogenesis, maintenance and dynamics of glycosomes in trypanosomatid parasites. Biochim Biophys Acta 1863:1038–1048CrossRefGoogle Scholar
  36. Hamada T, Nagasaki-Takeuchi N, Kato T, Fujiwara M, Sonobe S, Fukao Y, Hashimoto T (2013) Purification and characterization of novel microtubule-associated proteins from Arabidopsis cell suspension cultures. Plant Physiol 163:1804–1816CrossRefPubMedGoogle Scholar
  37. Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16:241–256CrossRefPubMedGoogle Scholar
  38. Herman PL, Ramberg HA, Baack RD, Markwell J, Osterman JC (2002) Formate dehydrogenase in Arabidopsis thaliana: overexpression and subcellular localization in leaves. Plant Sci 163:1137–1145CrossRefGoogle Scholar
  39. Hooks MA, Allwood JW, Harrison JK, Kopka J, Erban A, Goodacre R, Balk J (2014) Selective induction and subcellular distribution of ACONITASE 3 reveal the importance of cytosolic citrate metabolism during lipid mobilization in Arabidopsis. Biochem J 463:309–317CrossRefGoogle Scholar
  40. Huang S, Jacoby RP, Millar AH, Taylor NL (2014) Plant mitochondrial proteomics. In: Jorrin-Novo J, Komatsu S, Weckwerth W, Wienkoop S (eds) Plant proteomics. Methods in molecular biology (methods and protocols), vol 1072. Humana Press, Totowa, NJGoogle Scholar
  41. Jiménez A, Romojaro F, Gómez JM, Llanos MR, Sevilla F (2003) Antioxidant systems and their relationship with the response of pepper fruits to storage at 20 °C. J Agric Food Chem 51:6293–6299CrossRefPubMedGoogle Scholar
  42. Joao HC, Williams RJ (1993) The anatomy of a kinase and the control of phosphate transfer. Eur J Biochem 216:1–18CrossRefPubMedGoogle Scholar
  43. Johnson TL, Olsen LJ (2003) Import of the peroxisomal targeting signal type 2 protein 3-ketoacyl-coenzyme A thiolase into glyoxysomes. Plant Physiol 133:1991–1999CrossRefPubMedGoogle Scholar
  44. Kaur N, Hu Y (2011) Defining the plant peroxisomal proteome: from Arabidopsis to rice. Front Plant Sci 2:103CrossRefPubMedGoogle Scholar
  45. Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjölander K, Gruissem W, Baginsky S (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr Biol 14:354–362CrossRefPubMedGoogle Scholar
  46. Kleiter AE, Gerhardt B (1998) Glyoxysomal β-oxidation of long-chain fatty acids: completeness of degradation. Planta 206:125–130CrossRefGoogle Scholar
  47. Kruft V, Eubel H, Jänsch L, Werhahn W, Braun H-P (2001) Proteomic approach to identify novel mitochondrial proteins in Arabidopsis. Plant Physiol 127:1694–1710CrossRefPubMedGoogle Scholar
  48. Kural C, Kim H, Syed S, Goshima G, Gelfand VI, Selvin PR (2005) Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement? Science 308:1469–1472CrossRefPubMedGoogle Scholar
  49. Li J, Xu Y, Chong K (2012) The novel functions of kinesin motor proteins in plants. Protoplasma 249(Suppl 2):S95–S100CrossRefGoogle Scholar
  50. Li L, Ban Z, Limwachiranon J, Luo Z (2017) Proteomic studies on fruit ripening and senescence. Crit Rev Plant Sci 36:116–127CrossRefGoogle Scholar
  51. Liepman AH, Olsen LJ (2001) Peroxisomal alanine: glyoxylate aminotransferase (AGT1) is a photorespiratory enzyme with multiple substrates in Arabidopsis thaliana. Plant J 25:487–498CrossRefGoogle Scholar
  52. López-Huertas E, del Río LA (2014) Characterization of antioxidant enzymes and peroxisomes of olive (Olea europaea L.) fruits. J Plant Physiol 171:1463–1471CrossRefGoogle Scholar
  53. Marondedze C, Gehring C, Thomas L (2014) Dynamic changes in the date palm fruit proteome during development and ripening. Hort Res 1:14039CrossRefGoogle Scholar
  54. Martí MC, Camejo D, Olmos E, Sandalio LM, Fernández-García N, Jiménez A, Sevilla F (2009) Characterisation and changes in the antioxidant system of chloroplasts and chromoplasts isolated from green and mature pepper fruits. Plant Biol 11:613–624CrossRefPubMedGoogle Scholar
  55. Martí MC, Camejo D, Vallejo F, Romojaro F, Bacarizo S, Palma JM, Sevilla F, Jiménez A (2011) Influence of fruit ripening stage and harvest period on the antioxidant content of sweet pepper cultivars. Plant Foods Hum Nutr 66:416–423CrossRefPubMedGoogle Scholar
  56. Mateos RM, León AM, Sandalio LM, Gómez M, del Río LA, Palma JM (2003) Peroxisomes from pepper fruits (Capsicum annuum L): Purification, characterization and antioxidant activity. J Plant Physiol 160:1507–1516CrossRefGoogle Scholar
  57. Mateos RM, Bonilla-Valverde D, del Río LA, Palma JM, Corpas FJ (2009) NADP-dehydrogenases from pepper fruits: effect of maturation. Physiol Plant 135:130–139CrossRefPubMedGoogle Scholar
  58. Mateos RM, Jiménez A, Román P, Romojaro F, Bacarizo S, Leterrier M, Gómez M, Sevilla F, del Río LA, Corpas FJ, Palma JM (2013) Antioxidant systems from pepper (Capsicum annuum L.): involvement in the response to temperature changes in ripe fruits. Int J Mol Sci 14:9556–9580CrossRefPubMedGoogle Scholar
  59. Mauseth JD (2003) Botany: an introduction to plant biology, 3rd edn. Jones and Bartlett Publishers, Sudbury, MassachusettsGoogle Scholar
  60. Millar AH (2007) The plant mitochondrial proteome. In: Šamaj J, Thelen JJ (eds) Plant proteomics. Springer, Berlin, HeidelbergGoogle Scholar
  61. Millar AH, Sweetlove LJ, Giegé P, Leave CJ (2001) Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol 127:1711–1727CrossRefPubMedGoogle Scholar
  62. Millar AH, Heazlewood JL, Kristensen BK, Braun HP, Møller IM (2005) The plant mitochondrial proteome. Trends Plant Sci 10:36–43CrossRefGoogle Scholar
  63. Minarik P, Tomaskova N, Kollarova M, Antalik M (2002) Malate dehydrogenases - structure and function. Gen Physiol Biophys 21:257–265Google Scholar
  64. Missihoun TD, Schmitz J, Klug R, Kirch HH, Bartels D (2011) Betaine aldehyde dehydrogenase genes from Arabidopsis with different sub-cellular localization affect stress responses. Planta 233:369–382CrossRefGoogle Scholar
  65. Muzio G, Maggiora M, Paiuzzi E, Oraldi M, Canuto RA (2012) Aldehyde dehydrogenases and cell proliferation. Free Radic Biol Med 52:735–746CrossRefGoogle Scholar
  66. Oeljeklaus S, Fischer K, Gerhardt B (2002) Glyoxysomal acetoacetyl-CoA thiolase and 3-oxoacyl-CoA thiolase from sunflower cotyledons. Planta 214:597–607CrossRefGoogle Scholar
  67. Offermann S, Okita TW, Edwards GE (2011) Resolving the compartmentation and function of C4 photosynthesis in the single-cell C4 species Bienertia sinuspersici. Plant Physiol 155:1612–1628CrossRefPubMedGoogle Scholar
  68. Okamura-Ikeda K, Hosaka H, Maita N, Fujiwara K, Yoshizawa AC, Nakagawa A, Taniguchi H (2010) Crystal structure of aminomethyltransferase in complex with dihydrolipoyl-H-protein of the glycine cleavage system: implications for recognition of lipoyl protein substrate, disease-related mutations, and reaction mechanism. J Biol Chem 285:18684–18692CrossRefPubMedGoogle Scholar
  69. Palma JM, López-Huertas E, Corpas FJ, Sandalio LM, Gómez M, del Río LA (1998) Peroxisomal manganese superoxide dismutase: purification and properties of the isozyme from pea leaves. Physiol Plant 104:720–726CrossRefGoogle Scholar
  70. Palma JM, Corpas FJ, del Río LA (2009) Proteome of plant peroxisomes: new perspectives on the role of these organelles in cell biology. Proteomics 9:2301–2312CrossRefGoogle Scholar
  71. Palma JM, Corpas FJ, del Río LA (2011) Proteomics as an approach to the understanding of the molecular physiology of fruit development and ripening. J Proteomics 74:1230–1243CrossRefGoogle Scholar
  72. Palma JM, Gupta DK, Corpas FJ (2013) Metalloenzymes involved in the metabolism of reactive oxygen species and heavy metals stress. In: Gupta DK, Corpas FJ, Palma JM (eds) Heavy metals stress in plants. Springer, Heidelberg, pp 1–17Google Scholar
  73. Palma JM, Sevilla F, Jiménez A, del Río LA, Corpas FJ, Álvarez de Morales P, Camejo DM (2015) Physiology of pepper fruit and the metabolism of antioxidants: chloroplasts, mitochondria and peroxisomes. Ann Bot 116:627–636CrossRefPubMedGoogle Scholar
  74. Pascual I, Azcona I, Aguirreolea J, Morales F, Corpas FJ, Palma JM, Rellán-Alvarez R, Sánchez-Díaz M (2010) Growth, yield, and fruit quality of pepper plants amended with two sanitized sewage sludges. J Agric Food Chem 58:6951–6959CrossRefGoogle Scholar
  75. Peterson GC, Sommer JM, Klosterman S, Wang CC, Parsons M (1997) Trypanosoma brucei: identification of an internal region of phosphoglycerate kinase required for targeting to glycosomal microbodies. Exp Parasitol 85:16–23CrossRefGoogle Scholar
  76. Pistelli L, Gerhardt B, Alpi A (1996) β-oxidation of fatty acids by the unspecialized peroxisomes from rice coleoptile. Plant Sci 118:25–30CrossRefGoogle Scholar
  77. Qin G, Wang Q, Liu J, Li B, Tian S (2009) Proteomic analysis of changes in mitochondrial protein expression during fruit senescence. Proteomics 9:4241–4253CrossRefGoogle Scholar
  78. Quan S, Yang P, Cassin-Ross G, Kaur N, Switzenberg R, Aung K, Li J, Hu J (2013) Proteome analysis of peroxisomes from etiolated Arabidopsis seedlings identifies a peroxisomal protease involved in β-oxidation and development. Plant Physiol 163:1518–1538CrossRefPubMedGoogle Scholar
  79. Reumann S (2002) The photorespiratory pathway of leaf peroxisomes. In: Baker A, Graham IA (eds) Plant peroxisomes: biochemistry, cell biology and biotechnological applications, Ed 1. Kluwer Academic Publishers, Dordreccht, The Netherlands, pp 141–189CrossRefGoogle Scholar
  80. Reumann S (2004) Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol 135:783–800CrossRefPubMedGoogle Scholar
  81. Reumann S (2011) Towards a definition of the complete proteome of plant peroxisomes: where experimental proteomics must be complemented by bioinformatics. Proteomics 11:1764–1779CrossRefPubMedGoogle Scholar
  82. Reumann S, Quan S, Aung K, Yang P, Manandhar-Shrestha K, Holbrook D, Linka N, Switzenberg R, Wilkerson CG, Weber AP, Olsen LJ, Hu J (2009) In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol 150:125–143CrossRefPubMedGoogle Scholar
  83. Rodríguez-Ruiz M, Álvarez de Morales P, Reumann S, Corpas FJ, Palma JM (2016) Peroxisomes from pepper fruits: new perspectives on the organelle metabolism. In: PerFuMe 2nd International Conference on Peroxisome Formation, Function and Metabolism, Hamburg, Germany. Abstract BookGoogle Scholar
  84. Rodríguez-Ruiz M, Mateos RM, Codesido V, Corpas FJ, Palma JM (2017a) Characterization of the galactono-1,4-lactone dehydrogenase from pepper fruits and its modulation in the ascorbate biosynthesis. Role of nitric oxide. Redox Biol. 12:171–181CrossRefPubMedGoogle Scholar
  85. Rodríguez-Ruiz M, Mioto P, Palma JM, Corpas FJ (2017b) S-nitrosoglutathione reductase (GSNOR) activity is down-regulated during pepper (Capsicum annuum L.) fruit ripening. Nitric Oxide 68:51–55CrossRefPubMedGoogle Scholar
  86. Rodríguez-Serrano M, Romero-Puertas MC, Pastori GM, Corpas FJ, Sandalio LM, del Río LA, Palma JM (2007) Peroxisomal membrane manganese superoxide dismutase: characterization of the isozyme from watermelon cotyledons. J Exp Bot 58:2417–2427CrossRefPubMedGoogle Scholar
  87. Rodríguez-Serrano M, Pazmiño DM, Sparkes I, Rochetti A, Hawes C, Romero-Puertas MC, Sandalio LM (2014) 2,4-Dichlorophenoxyacetic acid promotes S-nitrosylation and oxidation of actin affecting cytoskeleton and peroxisomal dynamics. J Exp Bot 65:4783–4793CrossRefPubMedGoogle Scholar
  88. Rodríguez-Serrano M, Romero-Puertas MC, Sanz-Fernández M, Hu J, Sandalio LM (2016) Peroxisomes extend peroxules in a fast response to stress via a reactive oxygen species-mediated induction of the peroxin PEX11a. Plant Physiol 171:1665–1674CrossRefPubMedGoogle Scholar
  89. Rosado D, Gramegna G, Cruz A, Lira BS, Freschi L, de Setta N, Rossi M (2016) Phytochrome interacting factors (PIFs) in Solanum lycopersicum: diversity, evolutionary history and expression profiling during different developmental processes. PLoS ONE 11:e0165929CrossRefPubMedGoogle Scholar
  90. Schuch W, Bird CR, Ray J, Smith CJ, Watson CF, Morris PC, Gray JE, Arnold C, Seymour GB, Tucker GA, Grierson D (1989) Control and manipulation of gene expression during tomato fruit ripening. Plant Mol Biol 13:303–311CrossRefPubMedGoogle Scholar
  91. Suzuki M, Takahashi S, Kondo T, Dohra H, Ito Y, Kiriiwa Y, Hayashi M, Kamiya S, Kato M, Fujiwara M, Fukao Y, Kobayashi M, Nagata N, Motohashi R (2015) Plastid proteomic analysis in tomato fruit development. PLoS ONE 10:e0137266CrossRefPubMedGoogle Scholar
  92. Szymanski J, Levin Y, Savidor A, Breitel D, Chappell-Maor L, Heinig U, Topfer N, Aharoni A (2017) Label-free deep shotgun proteomics reveals protein dynamics during tomato fruit tissues development. Plant J 90:396–417CrossRefPubMedGoogle Scholar
  93. Tamburino R, Vitale M, Ruggiero A, Sassi M, Sannino L, Arena S, Costa A, Batelli G, Zambrano N, Scaloni A, Grillo S, Scotti N (2017) Chloroplast proteome response to drought stress and recovery in tomato (Solanum lycopersicum L.). BMC Plant Biol 17:40CrossRefPubMedGoogle Scholar
  94. Thazar-Poulot N, Miquel M, Fobis-Loisy I, Gaude T (2015) Peroxisome extensions deliver the Arabidopsis SDP1 lipase to oil bodies. Proc Natl Acad Sci USA 112:4158–4163CrossRefGoogle Scholar
  95. Wang YQ, Yang Y, Fei Z, Yuan H, Fish T, Thannhauser TW, Mazourek M, Kochian LV, Wang X, Li L (2013) Proteomic analysis of chromoplasts from six crop species reveals insights into chromoplast function and development. J Exp Bot 64:949–961CrossRefPubMedGoogle Scholar
  96. Wang J, Yu Q, Xiong H, Wang J, Chen S, Yang Z, Dai S (2016) Proteomic insight into the response of Arabidopsis chloroplasts to darkness. PLoS ONE 11:e0154235CrossRefPubMedGoogle Scholar
  97. Wang L, Sun XL, Weiszmann J, Weckwerth W (2017) System-level and granger network analysis of integrated proteomic and metabolomic dynamics identifies key points of grape berry development at the interface of primary and secondary metabolism. Front Plant Sci 8:1066CrossRefPubMedGoogle Scholar
  98. Wu XQ, Jiang L, Yu M, An X, Ma R, Yu Z (2016) Proteomic analysis of changes in mitochondrial protein expression during peach fruit ripening and senescence. J Proteomics 147:197–211CrossRefPubMedGoogle Scholar
  99. Yurimoto H, Lee B, Yasuda F, Sakai Y, Kato N (2004) Alcohol dehydrogenases that catalyse methyl formate synthesis participate in formaldehyde detoxification in the methylotrophic yeast Candida boidinii. Yeast 21:341–350CrossRefPubMedGoogle Scholar
  100. Zhu XD, Zhang CB, Wu WM, Li XP, Zhang CA, Fang JG (2017) Enzyme activities and gene expression of starch metabolism provide insights into grape berry development. Hort Res 4:17018CrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Group of Antioxidants, Free Radicals and Nitric Oxide in Biotechnology, Food and AgricultureEstación Experimental del ZaidínGranadaSpain

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