Nitric oxide prevents wound-induced browning and delays senescence through inhibition of hydrogen peroxide accumulation in fresh-cut lettuce

Innovative Food Science and Emerging Technologies

Volumn 30, Issue , 2015, Pages 157-169

  Iakimova, Elena T ^a,b   Woltering, Ernst J ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b Institute of Ornamental and Medicinal Plants   (Bulgaria)

Author keywords

Browning; Cell death; Fresh cut lettuce; Hydrogen peroxide; Nitric oxide; Wounding

Indexed keywords

CELL DEATH; CELLS; HYDROGEN PEROXIDE; NITRIC OXIDE; OXIDATION; OXIDATIVE STRESS; PEROXIDES; PHYSIOLOGICAL MODELS; PLANTS (BOTANY); SEA ICE;

BIOACTIVE INGREDIENTS; BROWNING; FRESH-CUT LETTUCE; MORPHOLOGICAL MARKERS; PHYSIOLOGICAL PROCESS; POST-PROCESSING CONDITION; TECHNOLOGICAL SOLUTION; WOUNDING;

CYTOLOGY;

EID: 84947042149     PISSN: 14668564     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ifset.2015.06.001     Document Type: Article

References (98)

1. A. Allende, and F. Artes UV-C radiation as a novel technique for keeping quality of fresh processed 'Lollo Rosso' lettuce Food Research International 36 2003 739 746
2. J.M. Amiot, A. Fleuriet, C. Veronique, and J. Nicolas Phenolic compounds and oxidative mechanism in fruit and vegetables. Phytochemistry of fruit and vegetables F.A. Tomas-Barberan, R.J. Robins, Proceeding of the Phytochemical Society of Europe 1997 Clarendon Press Oxford, UK 51 85
3. A. Ballantyne, R. Stark, and J.D. Selman Modified atmosphere packaging of shredded lettuce International Journal of Food Science and Technology 23 1988 267 274
4. D.M. Barrett, J.C. Beaulieu, and R. Shewfelt Color, flavor, texture, and nutritional quality of fresh-cut fruits and vegetables: Desirable levels, instrumental and sensory measurement, and the effects of processing Critical Reviews in Food Science and Nutrition 50 2010 369 389
5. J.S. Beckman, and W.H. Koppenol Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and the ugly American Journal of Physiology. Cell Physiology 271 5 1996 C1424 C1437
6. H.R. Bolin, A.E. Stafford, J.R.A.D. King, and C.C. Huxsoll Factors affecting the storage stability of shredded lettuce Journal of Food Science 42 1997 1319 1321
7. 2 synthesis The Plant Journal 45 2006 113 122
8. V. Buchanan-Wollaston, S. Earl, E. Harrison, E. Mathas, S. Navabpour, T. Page, and et al. The molecular analysis of leaf senescence - A genomics approach Plant Biotechnology Journal 1 2003 3 22
9. R.C. Caldwell Alkylperoxyl radical scavenging activity of red leaf lettuce (Lactuca sativa L.) phenolics Journal of Agricultural and Food Chemistry 51 2003 4589 4595
10. R. Campos-Vargas, and M.E. Saltveit Involvement of putative chemical wound signals in the induction of phenolic metabolism in wounded lettuce Physiologia Plantarum 114 2002 73 84
11. M. Cantwell, and T. Suslow Fresh-cut fruits and vegetables: Aspects of physiology, preparation and handling that affect quality Fresh-cut products: Maintaining quality and safety UCDavis Extension, Section 4B 2004
12. M. Castañer, M.I. Gil, F. Asrtes, and F.A. Tomas-Barberan Inhibition of browning of harvested head lettuce Journal of Food Science 61 1996 314 316
13. S.A. Coupe, B.K. Sinclair, M. Watson, J.A. Heyes, and J.R. Eason Identification of dehydration-responsive cysteine proteases during postharvest senescence of broccoli florets Journal of Experimental Botany 54 2003 1045 1056
14. R. Couture, M.I. Cantwell, D. Ke, and M.E. Saltveit Physiological attributes related to quality attributes and storage life of minimally processed lettuce HortScience 58 1993 609 610
15. J.-X. Cui, Y.-H. Zhou, J.-G. Ding, X.-J. Xia, K. Shi, S.-C. Chen, and et al. Role of nitric oxide in hydrogen peroxide-dependent induction of abiotic stress tolerance by brassinosteroids in cucumber Plant, Cell & Environment 34 2011 347 358
16. E. Degl'Innocenti, L. Guidi, A. Pardossi, and F. Tognoni Biochemical study of leaf browning in minimally processed leaves of lettuce (Lactuca sativa L. var. acephala) Journal of Agricultural and Food Chemistry 53 2005 9980 9984
17. E. Degl'Innocenti, A. Pardossi, F. Tognoni, and L. Guidi Physiological basis of sensitivity to enzymatic browning in 'lettuce', 'escarole' and 'rocket salad' when stored as fresh-cut products Food Chemistry 104 2007 209 215
18. M. Delledonne, Y. Xia, R.A. Dixon, and C. Lamb Nitric oxide functions as a signal in plant defense resistance Nature 394 1998 585 588
19. J. Dong, M. Zhang, L. Lu, L. Sun, and M. Xu Nitric oxide fumigation stimulates flavonoid and phenolic accumulation and enhances antioxidant activity of mushroom Food Chemistry 135 2012 1220 1225
20. X. Duan, X. Su, Y. You, H. Qu, Y. Li, and Y. Jiang Effect of nitric oxide on pericarp browning of harvested longan fruit in relation to phenolic metabolism Food Chemistry 104 2007 571 576
21. J.R. Eason, D. Ryan, B. Page, L. Watson, and S.A. Coupe Harvested broccoli (Brassica oleracea) responds to high carbon dioxide and low oxygen atmosphere by inducing stress-response genes Postharvest Biology and Technology 43 2007 358 365
22. J. Floryszak-Wieczorek, G. Milczarek, M. Arasimowicz, and A. Ciszewski Do nitric oxide donors mimic endogenous NO-related response in plants? Planta 224 2006 1363 1372
23. S.C. Fonseca, F.A.R. Oiveira, and J.K. Brecht Modelling respiration rate of fresh fruits and vegetables for modified atmosphere packages: A review Journal of Food Engineering 52 2002 99 119
24. A. García, J.R. Mount, and P.M. Davison Ozone and chlorine treatment of minimally processed lettuce Food Microbiology and Safety 68 2003 2747 2751
25. M.I. Gil, J.A. Tudela, A. Martínez-Sánchez, and M.C. Luna Harvest maturity indicators of leafy vegetables Stewart Postharvest Review 8 2012 1 9(9)
26. S.S. Gill, and N. Tuteja Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants Plant Physiology and Biochemistry 48 2012 909 930
27. L.M. Guan, and J.G. Scandalios Hydrogen peroxide-mediated catalase gene expression in response to wounding Free Radical Biology & Medicine 28 2000 1182 1190
28. J.M. He, H. Xu, X.P. She, X.G. Song, and W.M. Zhao The role and interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broadbean Functional Plant Biology 32 2005 237 247
29. R. Hoque, R.B.H. Wills, and J.B. Golding Nitric oxide inhibits cut-surface browning in four lettuce types The Journal of Horticultural Science and Biotechnology 86 2011 97 100
30. D.J. Huber Postharvest senescence: An introduction to the symposium HortScience 22 1987 853 859
31. M. Iriti, M. Sironi, S. Gomarasca, A.P. Casazza, C. Soave, and F. Faoro Cell death-mediated antiviral effect of chitosan in tobacco Plant Physiology and Biochemistry 44 2006 893 900
32. T. Jabs Reactive oxygen intermediates as mediators of programmed cell death in plants and animals Biochemical Pharmacology 57 1999 231 245
33. E.G. Janzen, A.L. Wilcox, and V. Manoharant Reactions of nitric oxide with phenolic antioxidants and phenoxy1 radicals The Journal of Organic Chemistry 58 1993 3597 3599
34. T. Jiang, X. Zheng, J. Li, G. Jing, L. Cai, and T. Ying Integrated application of nitric oxide and modified atmosphere packaging to improve quality retention of button mushroom (Agaricus bisporus) Food Chemistry 126 2011 1693 1699
35. A.A. Kader, W.J. Lipton, and L.L. Morris Systems for scoring quality of harvested lettuce HortScience 8 5 1973 408 409
36. A.A. Kader, and M.E. Saltveit Atmosphere modification J.A. Bartz, J.K. Brecht, Postharvest physiology and pathology of vegetables 2003 Marcel Dekker New York 229 246
37. Ho.-M. Kang, and M.E. Saltveit Antioxidant capacity of lettuce leaf tissue increases after wounding Journal of Agriculture and Food Chemistry 50 2002 7536 7541
38. Ho.-M. Kang, and M.E. Saltveit Wound-induced increases in phenolic content of fresh-cut lettuce is reduced by a short immersion in aqueous hypertonic solutions Postharvest Biology and Technology 29 2003 271 277
39. S. Karpinski, B. Reynolds, B. Karpinska, G. Wingsle, G. Creissen, and P. Mullineaux The role of hydrogen peroxide and antioxidants in systemic acclimation to photooxidative stress in Arabidopsis M.F. Smallwood, C.M. Calvert, D.J. Bowles, Plant responses to environmental stress 1999 Bios Scientific Publishers Oxford 25 32
40. C. Kaur, and H.C. Kapoor Antioxidants in fruits and vegetables the millennium's health International Journal of Food Science and Technology 36 2001 703 725
41. R.C. Keogh, B.J. Deverall, and S. Mcleod Comparison of histological and physiological responses to Phakopsora pachyrhizi in resistant and susceptible soybean Transactions of the British Mycological Society 74 1980 329 333
42. G.A. King, D.C. Woollard, D.E. Irving, and W.M. Borst Physiological changes in asparagus tips after harvest Physiologia Plantarum 80 1990 393 400
43. L. Lamattina, C. Garcia-Mata, M. Graziano, and G. Pagnussat Nitric oxide: The versatility of an extensive signal molecule Annual Review of Plant Biology 54 2003 109 136
44. C. Lamb, and R.A. Dixon The oxidative burst in plant disease resistance Annual Review of Plant Physiology and Plant Molecular Biology 48 1997 251 275
45. J. León, E. Rojo, and J.J. Sánchez-Serrano Wound signalling in plants Journal of Experimental Botany 52 2001 1 9
46. Y.Y. Leshem, R.B.H. Wills, and V.V.V. Ku Evidence for the function of the free radical gas - Nitric oxide (NO) as an endogenous maturation and senescence regulating factor in higher plants Plant Physiology and Biochemistry 36 1998 825 833
47. A. Levine, R.I. Pennell, M.E. Alvarez, R. Palmer, and C.J. Lamb Calcium-mediated apoptosis in plant hypersensitive disease resistance response Current Biology 6 1996 427 437
48. 2 from the oxidative burst orchestrates the plant hypersensitive response Cell 79 1994 583 593
49. K.-H. Lin, M.-Y. Huang, W.-D. Huang, M.-H. Hsu, Z.-W. Yang, and C.-M. Yang The effects of red, blue, and white light-emitting diodes on the growth, development, and edible quality of hydroponically grown lettuce (Lactuca sativa L. var. capitata) Scientia Horticulturae 150 2013 86 91
50. R. Llorach, A. Martínez-Sánchez, F.A. Tomás-Barberán, M.I. Gil, and F. Ferreres Characterisation of polyphenols and antioxidant properties of five lettuce varieties and escarole Food Chemistry 108 2008 1028 1038
51. J.G. Loaiza-Velarde, F.A. Tomás-Barberá, and M.E. Salveit Effect of intensity and duration of heat-shock treatments on wound-induced phenolic metabolism in iceberg lettuce Journal of the American Society for Horticultural Science 122 1997 873 877
52. G. López-Gálvez, M. Saltveit, and M. Cantwell Wound-induced phenylalanine ammonia lyase activity: Factors affecting its induction and correlation with the quality of minimally processed lettuces Postharvest Biology and Technology 9 1996 223 233
53. G. López-Gálvez, M. Salveit, and M. Cantwell The visual quality of minimally processed lettuce stored in air and controlled atmosphere with emphasis on romaine and iceberg types Postharvest Biology and Technology 8 1996 179 190
54. H.K. Lum, Y.K.C. Butt, and S.C.L. Lo Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Phaseolus aureus) Nitric oxide: Biology and chemistry 6 2002 205 213
55. A.B. Martín-Diana, D. Rico, and C. Barry-Ryan Green tea extract as a natural antioxidant to extend the shelf-life of fresh-cut lettuce Innovative Food Science & Emerging Technologies 9 2008 593 603
56. A. Martínez-Sánchez, M.C. Luna, M.V. Selma, J.A. Tudela, J. Abad, and M.I. Gil Baby-leaf and multi-leaf of green and red lettuces are suitable raw materials for the fresh-cut industry Postharvest Biology and Technology 63 2012 1 10
57. T.E. Mishina, C. Lamb, and J. Zeier Expression of a nitric oxide degrading enzyme induces a senescence programme in Arabidopsis Plant, Cell & Environment 30 2007 39 52
58. R. Mittler, E.H. Herr, B.L. Orvar, W. van Camp, H. Willekens, and B.E. Ellis Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection Proceedings of the National Academy of Sciences of the United States of America 96 1999 14165 14170
59. L.A.J. Mur, I.E. Santosa, J.J. Laarhoven, N.J. Holton, F.J.M. Harren, and A.R. Smith Laser photoacoustic detection allows in planta detection of nitric oxide in tobacco following challenge with avirulent and virulent Pseudomonas syringae pathovars Plant Physiology 138 2005 1247 1258
60. S.J. Neill, R. Desikan, A. Clarke, R.D. Hurst, and J.T. Hancock Hydrogen peroxide and nitric oxide as signalling molecules in plants Journal of Experimental Botany 53 2002 1237 1247
61. S.J. Neill, R. Desikan, and J.T. Hancock Nitric oxide signalling in plants New Phytologist 159 2003 11 35
62. C. Nicolle, N. Cardinault, E. Gueux, L. Jaffrelo, E. Rock, A. Mazur, and et al. Health effect of vegetable-based diet: Lettuce consumption improves cholesterol metabolism and antioxidant status in the rat Clinical Nutrition 23 2004 605 614
63. C. Nicolle, A. Carnat, D. Fraisse, J.-L. Lamaison, E. Rock, H. Michel, and et al. Characterisation and variation of antioxidant micronutrients in lettuce (Lactuca sativa folium) Journal of the Science of Food and Agriculture 84 2004 2061 2069
64. M.L. Orozco-Cárdenas, J. Narváez-Vásquez, and C.A. Ryan Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate Plant Cell 13 2001 179 191
65. L. Pereyra, S.I. Roura, and C.E. del Valle Phenylalanine ammonia lyase activity in minimally processed Romaine lettuce Food Science and Technology 38 2005 67 72
66. I. Perucka, and K. Olszówka Effect of foliar calcium chloride treatment on the level of chlorogenic acid, β-carotene, lutein and tocopherols Acta Agrobotanica 64 2011 65 72
67. T.K. Prasad, M.D. Anderson, B.A. Martin, and C.R. Stewart Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide Plant Cell 6 1994 65 74
68. P. Pristijono, R.B.H. Wills, and J.B. Golding Inhibition of browning on the surface of apple slices by short term exposure to nitric oxide (NO) gas Postharvest Biology and Technology 42 2006 256 259
69. D. Rico, A.B. Martín-Diana, J. Henehan, G.T.M. Frías, and C. Barry-Ryan Effect of ozone and calcium lactate treatments on browning and textured properties of fresh-cut lettuce Journal of Food Science and Agriculture 86 2006 2179 2188
70. P. Rockel, F. Strube, A. Rockel, J. Wildt, and W.M. Kaiser Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro Journal of Experimental Botany 53 2002 103 110
71. M.E. Saltveit The rate of ion leakage from chilling-sensitive tissue does not immediately increase upon exposure to chilling temperatures Postharvest Biology and Technology 26 2002 295 304
72. M.E. Saltveit Effect of 1-methylcyclopropene on phenylpropanoid metabolism, the accumulation of phenolic compounds, and browning of whole and fresh-cut 'iceberg' lettuce Postharvest Biology and Technology 34 2004 75 80
73. M.E. Saltveit, and Y.-J. Choi Aromatic- and di-carboxylates inhibit wound-induced phenolic accumulation in excised lettuce (Lactuca sativa L.) leaf tissue Postharvest Biology and Technology 46 2007 222 229
74. M.E. Saltveit, O. Ochoa, R. Campos-Vargas, and R. Michelmore Lines of lettuce selected for ethylene insensitivity at the seedling stage displayed variable responses to ethylene or wounding as mature heads Postharvest Biology and Technology 27 2003 277 283
75. 2 partial pressure on respiration and quality Journal of Agriculture and Food Chemistry 46 1998 4556 4562
76. L. Soegiarto, R.B.H. Wills, J.A. Seberry, and Y.Y. Leshem Nitric oxide degradation in oxygen atmospheres and rate of uptake by horticultural produce Postharvest Biology and Technology 28 2003 327 331
77. J.Y. Song, D.S. Kim, M.-C. Lee, K.J. Lee, J.-B. Kim, S.H. Kim, and et al. Physiological characterization of gamma-ray induced salt tolerant rice mutants Australian Journal of Crop Science 6 3 2012 421 429
78. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction The Plant Journal 11 1997 1187 1194
79. W.G. Van Doorn, and E.J. Woltering Senescence and programmed cell death: Substance or semantics? Journal of Experimental Botany 55 2004 2147 2153
80. W.G. van Doorn, and E.J. Woltering Many ways to exit? Cell death categories in plants Trends in Plant Science 10 2005 117 122
81. A.F. Vanin, D.A. Svistunenko, V.D. Mikoyan, V.A. Serezhenkov, M.J. Fryer, N.R. Baker, and et al. Endogenous superoxide production and the nitrite/nitrate ratio control the concentration of bioavailable free nitric oxide in leaves Journal of Biological Chemistry 279 2004 24100 24107
82. C. Wagstaff, G.J.J. Clarkson, S.D. Rothwell, A. Page, G. Taylor, and M.S. Dixon Characterisation of cell death in bagged baby salad leaves Postharvest Biology and Technology 46 2007 150 159
83. 2-induced leaf cell death and the crosstalk of reactive nitric/oxygen species Journal of Integrative Plant Biology 55 2013 202 208
84. D. Wendehenne, J. Durner, and D.F. Klessig Nitric oxide: A new player in plant signalling and defence responses Current Opinion in Plant Biology 7 2004 449 455
85. D.C. Wildon, J.F. Thain, P.E.H. Minchin, I.R. Gubb, A.J. Reilly, Y.D. Skipper, and et al. Electrical signalling and systemic proteinase inhibitor induction in the wounded plant Nature 360 1992 62 65
86. R.B.H. Wills, P. Pristijono, and J.B. Golding Browning on the surface of cut lettuce slices inhibited by short term exposure to nitric oxide (NO) Food Chemistry 107 2008 1387 1392
87. I. Witkowska, and E.J. Woltering Pre-harvest light intensity affects shelf-life of fresh-cut lettuce Acta Horticulturae 877 2010 223 227
88. I.M. Witkowska, and E.J. Woltering Plant age affects wound-induced senescence in Lactuca sativa L. Journal of Plant Biochemistry and Physiology 2 2013 119 10.4172/2329-9029.1000119
89. I.M. Witkowska, and E.J. Woltering Storage of intact heads prior to processing limits the shelf-life of fresh-cut Lactuca sativa L. Postharvest Biology and Technology 91 2014 25 31
90. E.J. Woltering, and E.T. Iakimova Programmed cell death and postharvest deterioration of horticultural produce Acta Horticulturae 877 2010 991 998
91. E.J. Woltering, and Y.W. Seifu Low intensity monochromatic red, blue or green light increases the carbohydrate levels and substantially extends the shelf life of fresh-cut lettuce Acta Horticulturae 1079 2015 257 264
92. B.W. Yun, A. Feechan, M. Yin, N.B. Saidi, T. Le Bihan, M. Yu, and et al. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity Nature 478 2011 264 268
93. J. Zeier, M. Delledonne, T. Mishina, E. Severi, M. Sonoda, and C. Lamb Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions Plant Physiology 136 2004 2875 2886
94. L. Zhan, J. Hu, Z. Ai, L. Pang, Y. Li, and M. Zhu Light exposure during storage preserving soluble sugar and l-ascorbic acid content of minimally processed romaine lettuce (Lactuca sativa L. var. longifolia) Food Chemistry 136 2013 273 278
95. L. Zhan, Y. Li, J. Hu, L. Pang, and H. Fan Browning inhibition and quality preservation of fresh-cut romaine lettuce exposed to high intensity light Innovative Food Science & Emerging Technologies 14 2012 70 76
96. A.Y. Zhang, M.Y. Jiang, J.H. Zhang, H.D. Ding, S.C. Xu, X.L. Hu, and et al. Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen activated protein kinase cascade involved in antioxidant defence in maize leaves New Phytologist 175 2007 36 50
97. S.H. Zhu, and J. Zhou Effect of nitric oxide on ethylene production in strawberry fruit during storage Food Chemistry 100 2007 1517 1522
98. L.-Q. Zhu, J. Zhou, S.-H. Zhu, and L.-H. Guo Inhibition of browning on the surface of peach slices by short-term exposure to nitric oxide and ascorbic acid Food Chemistry 114 2009 174 179