Towards understanding vacuolar antioxidant mechanisms: A role for fructans?

Journal of Experimental Botany

Volumn 64, Issue 4, 2013, Pages 1025-1038

  Peshev, Darin ^a   Vergauwen, Rudy ^a   Moglia, Andrea ^b   Hideg, Éva ^c   Van Den Ende, Wim ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF PÉCS   (Hungary)

Author keywords

Fructan; phenols; radicals; ROS; stress; sugars; vacuole

Indexed keywords

ANTIOXIDANT; DISACCHARIDE; FENTON'S REAGENT; FRUCTAN; HYDROGEN PEROXIDE; HYDROXYL RADICAL; INULOBIOSE; IRON; PHENOL DERIVATIVE; PLANT EXTRACT; SUCROSE; SUPEROXIDE;

ARTICLE; CELL VACUOLE; CHEMICAL STRUCTURE; CHEMISTRY; CHICORY; CYTOSOL; INTRACELLULAR MEMBRANE; OXIDATIVE STRESS; PLANT LEAF;

ANTIOXIDANTS; CHICORY; CYTOSOL; DISACCHARIDES; FRUCTANS; HYDROGEN PEROXIDE; HYDROXYL RADICAL; INTRACELLULAR MEMBRANES; IRON; MOLECULAR STRUCTURE; OXIDATIVE STRESS; PHENOLS; PLANT EXTRACTS; PLANT LEAVES; SUCROSE; SUPEROXIDES; VACUOLES;

EID: 84874747779     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ers377     Document Type: Article

References (72)

1. Amiard V, Morvan-Bertrand A, Billard JP, Huault C, Keller F, Prud'homme MP. 2003. Fructans, but not the sucrosyl-galactosides, raffinose and loliose, are affected by drought stress in perennial ryegrass. Plant Physiology 132, 2218-2229. (Pubitemid 37024181)
2. Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373-399. (Pubitemid 38940937)
3. Awika JM, Rooney LW, Wu XL, Prior RL, Cisneros-Zevallos L. 2003. Screening methods to measure antioxidant activity of sorghum (Sorghum bicolor) and sorghum products. Journal of Agricultural and Food Chemistry 51, 6657-6662.
4. Benaroudj N, Lee DH, Goldberg AL. 2001. Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. Journal of Biological Chemistry 276, 24261-24267.
5. Blokhina O, Virolainen E, Fagerstedt KV. 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany 91, 179-194.
6. Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W. 2010. Sugar signalling and antioxidant network connections in plant cells. FEBS Journal 277, 2022-2037.
7. Bolouri Moghaddam MR, Van den Ende W. 2012. Sugars and plant innate immunity. Journal of Experimental Botany 63, 3989-3998.
8. Boyer JS. 1982. Plant productivity and environment. Science 218, 443-448.
9. Bradford MM. 1976. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
10. Carter C, Pan SQ, Jan ZH, Avila EL, Girke T, Raikhel NV. 2004. The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. The Plant Cell 16, 3285-3303. (Pubitemid 41096007)
11. Choudhary MI, Begum A, Abbaskhan A, Shafiq-ur R, Atta-ur R. 2006. Cinnamate derivatives of fructo-oligosaccharides from Lindelofia stylosa. Carbohydrate Research 341, 2398-2405. (Pubitemid 44294877)
12. Costa MMR, Hilliou F, Duarte P, Pereira LG, Almeida I, Leech M, Memelink J, Barcelo AR, Sottomayor M. 2008. Molecular cloning and characterization of a vacuolar class III peroxidase involved in the metabolism of anticancer alkaloids in Catharanthus roseus. Plant Physiology 146, 2403-2417.
13. Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K. 2011. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biology 11, 163.
14. Czapski G. 1984. Reaction of OH. Methods in Enzymology 105, 209-215.
15. Elstner EF, Osswald W. 1994. Mechanisms of oxygen activation during plant stress. Proceedings of the Royal Society of Edinburgh Section B: Biological Sciences 102, 131-154.
16. 2 affair? Journal of Experimental Botany 62, 2841-2854.
17. Foyer CH, Shigeoka S. 2011. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiology 155, 93-100.
18. Fry SC, Dumville JC, Miller JG. 2001. Fingerprinting of polysaccharides attacked by hydroxyl radicals in vitro and in the cell walls of ripening pear fruit. Biochemical Journal 357, 727-739.
19. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C. 2006. Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28, 1091-1101. (Pubitemid 44714119)
20. Gomez-Ariza J, Campo S, Rufat M, Estopa M, Messeguer J, San Segundo B, Coca M. 2007. Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesis-related PRms protein in rice plants. Molecular Plant-Microbe Interactions 20, 832-842. (Pubitemid 46944976)
21. Habila JD, Bello IA, Dzikwi AA, Musa H, Abubakar N. 2010. Total phenolics and antioxidant activity of Tridax procumbens Linn. African Journal of Pharmacy and Pharmacology 4, 123-126.
22. Hernandez-Marin E, Martínez A. 2012. Carbohydrates and their free radical scavenging capability: a theoretical study. Journal of Physical Chemistry B 116, 9668-9675.
23. Hincha DK, Zuther E, Heyer AG. 2003. The preservation of liposomes by raffinose family oligosaccharides during drying is mediated by effects on fusion and lipid phase transitions. Biochimica et Biophysica Acta 1612, 172-177. (Pubitemid 36629571)
24. Innocenti M, Gallori S, Giaccherini C, Ieri F, Vincieri FF, Mulinacci N. 2005. Evaluation of the phenolic content in the aerial parts of different varieties of Cichorium intybus L. Journal of Agricultural and Food Chemistry 53, 6497-6502. (Pubitemid 41169404)
25. Jamieson DJ. 1998. Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14, 1511-1527. (Pubitemid 29015366)
26. Jang JC, Sheen J. 1994. Sugar sensing in higher-plants. The Plant Cell 6, 1665-1679.
27. Kazak H, Toksoy Öner E, Barbosa EM, Dekker RFH, Khaper N. 2011. Biological significance of levan and glucan type exopolysaccharides in pancreatic cells. Poster presented at the International Heart Conference, Winnipeg.
28. Lambeth JD. 2004. NOX enzymes and the biology of reactive oxygen. Nature Reviews Immunology 4, 181-189. (Pubitemid 38339084)
29. Le Roy K, Verhaest M, Rabijns A, Clerens S, Van Laere A, Van den Ende W. 2007. N-glycosylation affects substrate specificity of chicory fructan 1-exohydrolase: evidence for the presence of an inulin binding cleft. New Phytologist 176, 317-324. (Pubitemid 47480880)
30. Livingston DP, Hincha DK, Heyer AG. 2009. Fructan and its relationship to abiotic stress tolerance in plants. Cellular and Molecular Life Sciences 66, 2007-2023.
31. Moller IM. 2001. Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology 52, 561-591. (Pubitemid 33720048)
32. Müller K, Linkies A, Vreeburg RA, Fry S C, Krieger Liszkay A, Leubner Metzger G. 2009. In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiology 150, 1855-1865.
33. Neveu V, Perez-Jimenez J, Vos F, et al. 2010. Phenol-Explorer: an online comprehensive database on polyphenol contents in foods. Database (Oxford) 210, bpa024.
34. Nishizawa A, Yabuta Y, Shigeoka S. 2008. Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiology 147, 1251-1263. (Pubitemid 352844283)
35. Nuhse TS, Bottrill AR, Jones AME, Peck SC. 2007. Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. The Plant Journal 51, 931-940. (Pubitemid 47301663)
36. Passardi F, Penel C, Dunand C. 2004. Performing the paradoxical: how plant peroxidases modify the cell wall. Trends in Plant Science 9, 534-540. (Pubitemid 39408748)
37. Peshev D, Van den Ende W. 2012. Sugars as antioxidants in plants. In: Tuteja N, Gill SS, eds. Crop improvement under adverse conditions. New York: Springer Science + Business Media, 285-308.
38. Peters S, Egert A, Stieger B, Keller F. 2010. Functional identification of Arabidopsis ATSIP2 (At3g57520) as an alkaline alpha-galactosidase with a substrate specificity for raffinose and an apparent sink-specific expression pattern. Plant and Cell Physiology 51, 1815-1819.
39. 2 availability preferentially drives glutathione accumulation in vacuoles and chloroplasts. Plant, Cell and Environment 34, 21-32.
40. Ramel F, Sulmon C, Bogard M, Couee I, Gouesbet G. 2009. Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biology 9, 28.
41. Ritsema T, Brodmann D, Diks SH, Bos CL, Nagaraj V, Pieterse CMJ, Boller T, Wiemken A, Peppelenbosch MP. 2009. Are small GTPases signal hubs in sugar-mediated induction of fructan biosynthesis? PLoS One 4, e6605.
42. Rolland F, Baena-Gonzalez E, Sheen J. 2006. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Biology 57, 675-709. (Pubitemid 44061041)
43. Schneider T, Keller F. 2009. Raffinose in chloroplasts is synthesized in the cytosol and transported across the chloroplast envelope. Plant and Cell Physiology 50, 2174-2182.
44. Schopfer, P. 2001. Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. The Plant Journal 28, 679-88. (Pubitemid 34103157)
45. Shiomi N, Onodera S, Chatterton NJ, Harrison PA. 1991. Separation of fructooligosaccharide isomers by anion-exchange chromatography. Agricultural and Biological Chemistry 55, 1427-1428.
46. Singleton VL, Orthofer R, Lamuela-Raventos RM. 1999. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Oxidants and Antioxidants, A 299, 152-178. (Pubitemid 28483890)
47. Smeekens S, Ma J, Hanson J, Rolland F. 2010. Sugar signals and molecular networks controlling plant growth. Current Opinion in Plant Biology 13, 273-278.
48. Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P. 2006. Sucrosespecific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiology 140, 637-646. (Pubitemid 43956283)
49. Sottomayor M, Lopes Cardoso I, Pereira LG, Ros Barcelo A. 2004. Peroxidase and the biosynthesis of terpenoid indole alkaloids in the medicinal plant Catharanthus roseus (L.) G. Don. Phytochemistry Reviews 3, 159-171. (Pubitemid 41184547)
50. Soylemez T, von Sonntag C. 1980. Hydroxyl radical-induced oligomerization of ethylene in deoxygenated aqueous-solution. Journal of the Chemical Society-Perkin Transactions 2, 391-394.
51. Stoyanova S, Geuns J, Hideg E, Van den Ende W. 2011. The food additives inulin and stevioside counteract oxidative stress. International Journal of Food Sciences and Nutrition 62, 207-214.
52. Sulmon C, Gouesbet G, El Amrani A, Couee I. 2006. Sugarinduced tolerance to the herbicide atrazine in Arabidopsis seedlings involves activation of oxidative and xenobiotic stress responses. Plant Cell Reports 25, 489-498.
53. Takahama U. 2004. Oxidation of vacuolar and apoplastic phenolics substrates by peroxidase: physiological significance of the oxidation reactions. Phytochemistry Reviews 3, 207-219. (Pubitemid 41184550)
54. Tarczynski MC, Jensen RG, Bohnert HJ. 1993. Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259, 508-510. (Pubitemid 23058706)
55. Tavagnacco L, Engström O, Schnupf U, Saboungi M-L, Edward Himmel M, Widmalm G, Cesáro A, W Brady J. 2012. Caffeine and sugars interact in aqueous solutions: a simulation and NMR study. Journal of Physical Chemistry B 116, 11701-11711.
56. Tudella J, Nunes FM, Paradela R, Evtuguin DV, Domingues P, Amado F, Coimbra MA, Barros AIRNA, Domingues MRM. 2011. Oxidation of mannosyl oligosaccharides by hydroxyl radicals as assessed by electrospray mass spectrometry. Carbohydrate Research 346, 2603-2611.
57. Van den Ende W, De Coninck B, Clerens S, Vergauwen R, Van Laere A. 2003. Unexpected presence of fructan 6-exohydrolases (6-FEHs) in non-fructan plants: characterization, cloning, mass mapping and functional analysis of a novel 'cell-wall invertase-like' specific 6-FEH from sugar beet (Beta vulgaris L.). The Plant Journal 36, 697-710. (Pubitemid 37496496)
58. Van den Ende W, De Roover J, Van Laere A. 1996. In vitro synthesis of fructofuranosyl-only oligosaccharides from inulin and fructose by purified chicory root fructan:fructan fructosyl transferase. Physiologia Plantarum 97, 346-352. (Pubitemid 27098926)
59. Van den Ende W, Lammens W, Van Laere A, Schroeven L, Le Roy K. 2009. Donor and acceptor substrate selectivity among plant glycoside hydrolase family 32 enzymes. FEBS Journal 276, 5788-5798.
60. Van den Ende W, Peshev D, De Gara L. 2011. Disease prevention by natural antioxidants and prebiotics acting as ROS scavengers in the gastrointestinal tract. Trends in Food Science and Technology 22, 689-697.
61. Van den Ende W, Valluru R. 2009. Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? Journal of Experimental Botany 60, 9-18.
62. Vereyken IJ, Chupin V, Demel RA, Smeekens SCM, DeKruijff B. 2001. Fructans insert between the headgroups of phospholipids. Biochimica et Biophysica Acta 1510, 307-320. (Pubitemid 32149906)
63. Vergauwen R, Van den Ende W, Van Laere A. 2000. The role of fructan in flowering of Campanula rapunculoides. Journal of Experimental Botany 51, 1261-1266. (Pubitemid 30491477)
64. von Sonntag C. 2006. Carbon-centered radicals. In: Schreck S, ed. Free-radical-induced DNA damage and its repair: a chemical perspective. Heidelberg: Springer, 103-134.
65. Walling C. 1975. Fentons reagent revisited. Accounts of Chemical Research 8, 125-131.
66. Wang MF, Simon JE, Aviles IF, He K, Zheng QY, Tadmor Y. 2003. Analysis of antioxidative phenolic compounds in artichoke (Cynara scolymus L.). Journal of Agricultural and Food Chemistry 51, 601-608.
67. Whiteman S-A, Nuhse TS, Ashford DA, Sanders D, Maathuis FJM. 2008. A proteomic and phosphoproteomic analysis of Oryza sativa plasma membrane and vacuolar membrane. The Plant Journal 56, 146-156.
68. Wohlert J, Schnupf U, Brady JW. 2010. Free energy surfaces for the interaction of d-glucose with planar aromatic groups in aqueous solution. Journal of Chemical Physics 133, 155103.
69. Wiseman H, Halliwell B. 1996. Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochemical Journal 313, 17-29. (Pubitemid 26013419)
70. Wojtaszek P. 1997. Oxidative burst: an early plant response to pathogen infection. Biochemical Journal 322, 681-692. (Pubitemid 27135612)
71. Xiang L, Le Roy K, Bolouri-Moghaddam M-R, Vanhaecke M, Lammens W, Rolland F, Van den Ende W. 2011. Exploring the neutral invertase-oxidative stress defence connection in Arabidopsis thaliana. Journal of Experimental Botany 62, 3849-3862.
72. Zechmann B, Stumpe M, Mauch F. 2011. Immunocytochemical determination of the subcellular distribution of ascorbate in plants. Planta 233, 1-12.