Sugar signalling and antioxidant network connections in plant cells

FEBS Journal

Volumn 277, Issue 9, 2010, Pages 2022-2037

  Bolouri Moghaddam, Mohammad Reza ^a   Le Roy, Katrien ^b   Xiang, Li ^b   Rolland, Filip ^b   Van Den Ende, Wim ^b  

^a SARI AGRICULTURAL SCIENCES AND NATURAL RESOURCES UNIVERSITY   (Iran)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Antioxidant; Fructan; Hexokinase; Invertase; Mitochondria; Phenolic compounds; ROS scavenging; Senescence; Signalling; Sugar

Indexed keywords

ANTIOXIDANT; BETA FRUCTOFURANOSIDASE; FRUCTAN; GLUCOSE 6 PHOSPHATE; HEXOKINASE; HEXOKINASE 2; PHENOL DERIVATIVE; RAFFINOSE; REACTIVE OXYGEN METABOLITE; SUCROSE; SUCROSE SYNTHASE; SUGAR; TREHALOSE; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; CARBOHYDRATE ANALYSIS; CARBOHYDRATE METABOLISM; CELLULAR STRESS RESPONSE; CHLOROPLAST; CONCENTRATION (PARAMETERS); ENZYME ACTIVITY; LEAF SENESCENCE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION REACTION; PLANT CELL; PLANT STRESS; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SCAVENGING SYSTEM; SIGNAL TRANSDUCTION; SUCROSE METABOLISM; SUGAR TRANSPORT;

ANIMALS; ANTIOXIDANTS; CARBOHYDRATE METABOLISM; HUMANS; PLANTS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 77951243208     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07633.x     Document Type: Review

References (172)

1. Pego JV, Kortstee AJ, Huijser C Smeekens SCM (2000) Photosynthesis, sugars and the regulation of gene expression. J Exp Bot 51, 407 416. (Pubitemid 30104768)
2. Rolland F, Baena-Gonzalez E Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57, 675 709. (Pubitemid 44061041)
3. Ramon M, Rolland F Sheen J (2008) Sugar sensing and signaling. The Arabidopsis Book. American Society of Plant Biologists. doi :.
4. Rolland F, Winderickx J Thevelein JM (2001) Glucose sensing mechanisms in eukaryotic cells. Trends Biochem Sci 26, 310 317. (Pubitemid 32436381)
5. Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, Sauer N, Hall JL Williams LE (2003) The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 132, 821 829. (Pubitemid 36715081)
6. Essmann J, Schmitz-Thom I, Schon H, Sonnewald S, Weis E Scharte J (2008) RNA interference-mediated repression of cell wall invertase impairs defense in source leaves of tobacco. Plant Physiol 147, 1288 1299. (Pubitemid 352844287)
7. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141, 312 322. (Pubitemid 43974521)
8. Sohal RS Weindruch R (1996) Oxidative stress, caloric restriction, and aging. Science 273, 59 63. (Pubitemid 26255420)
9. Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39, 44 84. (Pubitemid 44566469)
10. Couée I, Sulmon C, Gouesbet G El Amrani A (2006) An involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57, 449 459. (Pubitemid 43164377)
11. Blokhina O, Virolainen E Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91, 179 194. (Pubitemid 36117177)
12. Powers SK Lennon SL (1999) Analysis of cellular responses to free radicals: focus on exercise and skeletal muscle. Proc Nutr Soc 58, 1025 1033.
13. Moller IM, Jensen PE Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58, 459 481. (Pubitemid 46986332)
14. Navabpour S, Morris K, Allen R, Harrison E, Mackerness S Buchanan-Wollaston V (2003) Expression of senescence enhanced genes in response to oxidative stress. J Exp Bot 54, 2285 2292. (Pubitemid 37231965)
15. Lim PO, Kim HJ Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58, 115 136.
16. Ramel F, Sulmon C, Bogard M, Couée 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 Biol 9, 28.
17. Van den Ende W Valluru R (2009) Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? J Exp Bot 60, 9 18.
18. Jang JC, Leon P, Zhou L Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9, 5 19. (Pubitemid 27144451)
19. Moore B, Zhou L, Rolland F, Hall Q, Cheng W-H, Liu Y-X, Hwang I, Jones T Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300, 332 336. (Pubitemid 36433725)
20. Chiou T Bush DR (1998) Sucrose is a signal molecule in assimilate partitioning. Plant Biol 95, 4784 4788. (Pubitemid 28207991)
21. Xiao W, Sheen J Jang JC (2000) The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol Biol 44, 451 461. (Pubitemid 32060745)
22. Vaughn MW, Harrington GN Bush DR (2002) Sucrose-mediated transcriptional regulation of sucrose symporter activity in the phloem. Proc Natl Acad Sci U S A 99, 10876 10880.
23. Wiese A, Elzinga N, Wobbes B Smeekens S (2004) A conserved upstream open reading frame mediates sucrose-induced repression of translation. Plant Cell 16, 1717 1729. (Pubitemid 38908771)
24. Solfanelli C, Poggi A, Loreti E, Alpi A Perata P (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140, 637 646. (Pubitemid 43956283)
25. Weber AP, Schwacke R Flugge UI (2005) Solute transporters of the plastid envelope membrane. Annu Rev Plant Biol 56, 133 164. (Pubitemid 40802406)
26. 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 (8 e6605, doi:.
27. Price J, Laxmi A, Martin SKS Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16, 2128 2150. (Pubitemid 39059733)
28. Palenchar PM, Kouranov A, Lejay LV Coruzzi GM (2004) Genome-wide patterns of carbon and nitrogen regulation of gene expression validate the combined carbon and nitrogen (CN)-signaling hypothesis in plants. Genome Biol 5, R91.
29. Bläsing OE, Gibon Y, Günther M, Höhne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible W-R Stitt M (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17, 3257 3281.
30. Li Y, Lee KK, Walsh S, Smith C, Hadingham S, Sorefan K, Cawley G Bevan MW (2006) Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a Relevance Vector Machine. Genome Res 16, 414 427. (Pubitemid 43327511)
31. Gutiérrez RA, Lejay LV, Dean A, Chiaromonte F, Shasha DE Coruzzi GM (2007) Qualitative network models and genomewide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol 8, R7. (Pubitemid 351910995)
32. Osuna D, Usadel B, Morcuende R, Gibon Y, Bläsing OE, Höhne M, Günter M, Kamlage B, Trethewey R, Scheible WR et al. (2007) Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J 49, 463 491. (Pubitemid 46146627)
33. Baena-González E, Rolland F, Thevelein JM Sheen J (2007) A central integrator of transcription networks in plant stress and energy signaling. Nature 448, 938 942. (Pubitemid 47312777)
34. Hendriks JH, Kolbe A, Gibon Y, Stitt M Geigenberger P (2003) ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol 133, 838 849. (Pubitemid 37325692)
35. Crevillén P, Ventriglia T, Pinto F, Orea A, Merida A Romero JM (2005) Differential pattern of expression and sugar regulation of Arabidopsis thaliana ADP-glucose pyrophosphorylase-encoding genes. J Biol Chem 280, 8143 8149. (Pubitemid 40349714)
36. Lunn JE, Feil R, Hendricks JHM, Gibon Y, Morcuende R, Osuna D, Scheible WR, Carillo P, Hajiresaei MR Stitt M (2006) Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397, 139 148. (Pubitemid 44032845)
37. Smith AM, Zeeman SC Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56, 73 98.
38. Ramon M Rolland F (2007) Plant development: introducing trehalose metabolism. Trends Plant Sci 12, 185 188. (Pubitemid 46722689)
39. Fujiki Y, Yoshikawa Y, Sato T, Inada N, Ito M, Nishida I Watanabe A (2001) Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiol Plant 111, 345 352. (Pubitemid 32169995)
40. Lee EJ, Koizumi N Sano H (2004) Identification of genes that are up-regulated in concert during sugar depletion in Arabidopsis. Plant Cell Environ 27, 337 345. (Pubitemid 38300540)
41. Leon P Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8, 110 116. (Pubitemid 36726466)
42. Yanagisawa S, Yoo SD Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signaling in plants. Nature 425, 521 525. (Pubitemid 37237048)
43. Daimon T, Taguchi T, Meng Y, Katsuma S, Mita K Shimada T (2008) Beta-fructofuranosidase genes of the silkworm, Bombyx mori: insights into enzymatic adaptation of B. mori to toxic alkaloids in mulberry latex. J Biol Chem 283, 15271 15279.
44. 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 J 276, 5788 5798.
45. Roitsch T Gonzalez MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9, 606 613. (Pubitemid 39558558)
46. Vargas WA, Pontis HG Salerno GL (2008) New insights on sucrose metabolism: evidence for an active A/N-Inv in chloroplasts uncovers a novel component of the intracellular carbon trafficking. Planta 227, 795 807.
47. Szarka A, Horemans N, Passarella S, Tarcsay Á, Örsi F, Salgó A Bánhegyi G (2008) Demonstration of an intramitochondrial invertase activity and the corresponding sugar transporters of the inner mitochondrial membrane in Jerusalem artichoke (Helianthus tuberosus L.) tubers. Planta 228, 765 775.
48. Lee HS Sturm A (1996) Purification and characterization of neutral and alkaline invertase from carrot. Plant Physiol 112, 1513 1522. (Pubitemid 27052465)
49. Sturm A, Hess D, Lee HS Lienhard S (1999) Neutral invertase is a novel type of sucrose-cleaving enzyme. Physiol Plant 107, 159 165. (Pubitemid 30003465)
50. Barratt DH, Derbyshire P, Findlay K, Pike M, Wellner N, Lunn J, Feil R, Simpson C, Maule AJ Smith AM (2009) Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase. Proc Natl Acad Sci U S A 106, 13124 13129.
51. Welham T, Pike J, Horst I, Flemetakis E, Katinakis P, Kaneko T, Sato S, Tabata S, Perry J, Parniske M et al. (2009) A cytosolic invertase is required for normal growth and cell development in the model legume, Lotus japonicus. J Exp Bot 60, 3353 3365.
52. Lou Y, Gou J-Y Xue H-W (2007) PIP5K9, an Arabidopsis phosphatidylinositol monophosphate kinase, interacts with a cytosolic invertase to negatively regulate sugar-mediated root growth. Plant Cell 19, 163 181. (Pubitemid 46852709)
53. Vargas W Salerno A (2009) The Cinderella story of sucrose hydrolysis: alkaline/neutral invertases, from cyanobacteria to unforeseen roles in plant cytosol and organelles. Plant Sci 178, 1 8, doi :.
54. Proels RK Roitsch T (2009) Extracellular invertase LIN6 of tomato: a pivotal enzyme for integration of metabolic, hormonal, and stress signals is regulated by a diurnal rhythm. J Exp Bot 60, 1555 1567.
55. Heyer AG, Raap M, Schroeer B, Marty B Willmitzer L (2004) Cell wall invertase expression at the apical meristem alters floral, architectural, and reproductive traits in Arabidopsis thaliana. Plant J 39, 161 169. (Pubitemid 38940807)
56. Gerrits N, Turk SCHJ, van Dun KPM, Hulleman SHD, Visser RGF, Weisbeek PJ Smeekens SCM (2001) Sucrose metabolism in plastids. Plant Physiol 125, 926 934. (Pubitemid 32169899)
57. Gerrits N (2000) Tuber-Specific Fructan Synthesis in Potato Amyloplasts. PhD Dissertation. Utrecht University
58. Balibrea Lara ME, Gonzalez Garcia MC, Fatima T, Ehness R, Lee TK, Proels R, Tanner W Roitsch T (2004) Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. Plant Cell 16, 1276 1287. (Pubitemid 38641520)
59. Silva MP Ricardo CPP (1992) β-fructosidases and in vitro dedifferentiation redifferentiation of carrot cells. Phytochemistry 31, 1507 1511.
60. Tang GQ, Luscher M Sturm A (1999) Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sucrose partitioning. Plant Cell 11, 177 189.
61. Weber H, Borisjuk L, Heim U, Buchner P Wobus U (1995) Seed coat-associated invertases of fava bean control both unloading and storage functions - Cloning of cDNAs and cell-type specific expression. Plant Cell 7, 1835 1846. (Pubitemid 3019802)
62. Wobus U Weber H (1999) Sugars as signal molecules in plant seed development. Biol Chem 380, 937 944. (Pubitemid 29412753)
63. Weschke W, Panitz R, Gubatz S, Wang Q, Radchuk R, Weber H Wobus U (2003) The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. Plant J 33, 395 411. (Pubitemid 36178007)
64. Kato-Noguchi H, Takaoka T Izumori K (2005) Psicose inhibits lettuce root growth via a hexokinase-independent pathway. Physiol Plant 125, 293 298. (Pubitemid 41565104)
65. De Coninck B, Le Roy K, Francis I, Clerens S, Vergauwen R, Halliday AM, Smith SM, Van Laere A Van den Ende W (2005) Arabidopsis AtcwINV3 and 6 are not invertases but are fructan exohydrolases (FEHs) with different substrate specificities. Plant Cell Environ 28, 432 443. (Pubitemid 40428330)
66. Le Roy K, Lammens W, Van Laere A Van den Ende W (2008) Influencing the binding configuration of sucrose in the active sites of chicory fructan 1-exohydrolase and sugar beet fructan 6-exohydrolase. New Phytol 178, 572 580. (Pubitemid 351550566)
67. Subbaiah CC, Palaniappan A, Duncan K, Rhoads DM, Huber SC Sachs MM (2006) Mitochondrial localization and putative signaling function of sucrose synthase in maize. J Biol Chem 281, 15625 15635. (Pubitemid 43848448)
68. Subbaiah CC, Huber SC, Sachs MM Rhoads DM (2007) Sucrose synthase: expanding protein function. Plant Signal Behav 2, 28 29.
69. Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52, 561 591. (Pubitemid 33720048)
70. Doudican NA, Song B, Shadel GS Doetsch PW (2005) Oxidative DNA damage causes mitochondrial genomic instability in Saccharomyces cerevisiae. Mol Cell Biol 25, 5196 5204. (Pubitemid 40781117)
71. Asada K (1999) The water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50, 601 639. (Pubitemid 129491975)
72. Sulmon C, Gouesbet G, El Amrani A Couée I (2006) Sugar-induced tolerance to the herbicide atrazine in Arabidopsis seedlings involves activation of oxidative and xenobiotic stress responses. Plant Cell Rep 25, 489 498.
73. Suzuki N Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126, 45 51.
74. Takahashi S Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13, 178 182.
75. Debnam PM, Fernie AR, Leisse A, Golding A, Bowsher CG, Grimshaw C, Knight JS Emes MJ (2004) Altered activity of the P2 isoform of plastidic glucose-6-phosphate dehydrogenase in tobacco (Nicotiana tabacum cv. Samsun) causes changes in carbohydrate metabolism and response to oxidative stress in leaves. Plant J 38, 49 59. (Pubitemid 38448443)
76. Vereyken IJ, van Kuik JA, Evers TH, Rijken PJ de Kruijff B (2003) Structural requirements of the fructan-lipid interaction. Biophys J 84, 3147 3154. (Pubitemid 36531762)
77. Passardi F, Penel C Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9, 534 540. (Pubitemid 39408748)
78. Dunand C, Crévecoeur M Penel C (2007) Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytol 174, 332 341. (Pubitemid 46457381)
79. Takahama U (2004) Oxidation of vacuolar and apoplastic phenolics substrates by peroxidase: physiological significance of the oxidation reactions. Phytochem Rev 3, 207 219. (Pubitemid 41184550)
80. Li X-M, Shi Y-H, Wang F, Wang H-S Le G-W (2007) In vitro free radical scavenging activities and effect of synthetic oligosaccharides on antioxidant enzymes and lipid peroxidation in aged mice. J Pharm Biomed Anal 43, 364 370. (Pubitemid 44856205)
81. Nishizawa A, Yukinori Y Shigeoka S (2008) Galactinol and raffinose as a novel function to protect plants from oxidative damage. Plant Physiol 147, 1251 1263. (Pubitemid 352844283)
82. Smirnoff N Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28, 1057 1060.
83. Morelli R, Russo-Volpe S, Bruno N Scalzo RL (2003) Fenton dependent damage to carbohydrates: free radical scavenging activity of some simple sugars. J Agric Food Chem 51, 7418 7425.
84. Morsy MR, Jouve L, Hausman JF, Hoffmann L McD Stewart J (2007) Alteration of oxidative and carbohydrate metabolism under abiotic stress in two rice (Oryza sativa L.) genotypes contrasting in chilling tolerance. J Plant Physiol 164, 157 167. (Pubitemid 46172506)
85. Buitink J, Hemminga MA Hoekstra FA (2000) Is there a role for oligosaccharides in seed longevity? An assessment of intracellular glass stability. Plant Physiol 122, 1217 1224. (Pubitemid 30221402)
86. Bailly C, Audigier C, Ladonne F, Wagner MH, Coste F, Corbineau F Côme D (2001) Changes in oligosaccharide content and antioxidant enzyme activities in developing bean seeds as related to acquisition of drying tolerance and seed quality. J Exp Bot 52, 701 708. (Pubitemid 32623712)
87. Lehner A, Bailly C, Flechel B, Poels P, Cume D Corbineau F (2006) Changes in wheat seed germination ability, soluble carbohydrate and antioxidant enzyme activities in the embryo during the desiccation phase of maturation. J Cereal Sci 43, 175 182. (Pubitemid 43181563)
88. Santarius KA (1973) The protective effect of sugars on chloroplast membranes during temperature and water stress and its relationship to frost, desiccation, and heat resistance. Planta 113, 105 114.
89. Agati G, Matteini P, Goti A Tattini M (2007) Chloroplast-located flavonoids can scavenge singlet oxygen. New Phytol 174, 77 89. (Pubitemid 46333290)
90. Hincha DK, Hellwege EM, Heyer AG Crowe JH (2000) Plant fructans stabilize phosphatidylcholine liposomes during freeze drying. Eur J Biochem 267, 535 540.
91. 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. Biochim Biophys Acta 1612, 172 177. (Pubitemid 36629571)
92. Parvanova D, Ivanov S, Konstantinova T, Karanov E, Atanassov A, Tsvetkov T, Alexieva V Djilianov D (2004) Transgenic tobacco plants accumulating osmolytes show reduced oxidative damage under freezing stress. Plant Physiol Biochem 42, 57 63. (Pubitemid 38106249)
93. Li HJ, Yang AF, Zhang XC, Gao F Zhang JR (2007) Improving freezing tolerance of transgenic tobacco expressing sucrose:sucrose 1- fructosyltransferase gene from Lactuca sativa. Plant Cell Tissue Organ Cult 89, 37 48. (Pubitemid 46623333)
94. Kawakami A, Sato Y Yoshida M (2008) Genetic engineering of rice capable of synthesizing fructans and enhancing chilling tolerance. J Exp Bot 59, 803 814. (Pubitemid 351644659)
95. De Gara L, de Pinto MC, Moliterni VMC D'Egidio MG (2003) Redox regulation and storage processes during maturation in kernels of Triticum durum. J Exp Bot 54, 249 258. (Pubitemid 36101161)
96. Paradiso A, Cecchini C, De Gara L D'Egidio MG (2006) Functional, antioxidant and rheological properties of meal from immature durum wheat. J Cereal Sci 43, 216 222. (Pubitemid 43181567)
97. Shen B, Jensen RG Bohnert HJ (1997) Mannitol protects against oxidation by hydroxyl radicals. Plant Physiol 115, 1211 1219. (Pubitemid 28395301)
98. Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2, 1027 1038. (Pubitemid 120015455)
99. Nery DCM, da Silva CG, Mariani D, Fernandes PN, Pereira MD, Panek AD Eleutherio ECA (2008) The role of trehalose and its transporter in protection against reactive oxygen species. Biochim Biophys Acta 1780, 1408 1411.
100. Müller J, Boller T Wiemken A (1995) Trehalose and trehalase in plants: recent developments. Plant Sci 112, 1 9. (Pubitemid 3008909)
101. Benaroudj N, Lee DH Goldberg AL (2001) Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J Biol Chem 276, 24261 24267. (Pubitemid 37410833)
102. Pereira EJ, Panek AD Eleutherio ECA (2003) Protection against oxidation during dehydration of yeast. Cell Stress Chaperones 8, 120 124.
103. Oku K, Watanabe H, Kubota M, Fukuda S, Kurimoto M, Tsujisaka Y, Komori M, Inoue Y Sakurai M (2003) NMR and quantum chemical study on the OH...pi and CH...O interactions between trehalose and unsaturated fatty acids: implication for the mechanism of antioxidant function of trehalose. J Am Chem Soc 125, 12739 12748. (Pubitemid 37280443)
104. Garg AK, Kim JK, Owens TG, Ranwala AP, Do Choi Y, Kochian LV Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci U S A 99, 15898 15903. (Pubitemid 35462720)
105. Granot D (2008) Putting plant hexokinases in their proper place. Phytochemistry 69, 2649 2654.
106. Galina A Seixas da Silva W (2000) Hexokinase activity alters sugar-nucleotide formation in maize homogenates. Phytochemistry 53, 29 37. (Pubitemid 30056843)
107. Contento AL, Kim S-J Bassham DC (2004) Transcriptome profiling of the response of Arabidopsis suspension culture cells to sucrose starvation. Plant Physiol 135, 2330 2347.
108. Olsson T, Thelander M Ronne H (2003) A novel type of chloroplast stromal hexokinase is the major glucose-phosphorylating enzyme in the moss Physcomitrella patens. J Biol Chem 278, 44439 44447. (Pubitemid 37377195)
109. da-Silva WS, Rezende GL Galina A (2001) Subcellular distribution and kinetic properties of cytosolic and non-cytosolic hexokinases in maize seedling roots: implications for hexose phosphorylation. J Exp Bot 52, 1191 1201. (Pubitemid 32646431)
110. Giese JO, Herbers K, Hoffmann M, Klosgen RB Sonnewald U (2005) Isolation and functional characterization of a novel plastidic hexokinase from Nicotiana tabacum. FEBS Lett 579, 827 831.
111. Cho JI, Ryoo N, Ko S, Lee SK, Lee J, Jung KH, Lee YH, Bhoo SH, Winderickx J, An G et al. (2006) Structure, expression, and functional analysis of the hexokinase gene family in rice (Oryza sativa L.). Planta 224, 598 611. (Pubitemid 44188103)
112. Kandel-Kfir M, Damari-Weissler H, German MA, Gidoni D, Mett A, Belausov E, Petreikov M, Adir N Granot D (2006) Two newly identified membrane-associated and plastidic tomato HXKs: characteristics, predicted structure and intracellular localization. Planta 224, 1341 1352. (Pubitemid 44769866)
113. Karve A, Rauh BL, Xia X, Kandasamy M, Meagher RB, Sheen J Moore BD (2008) Expression and evolutionary features of the hexokinase gene family in Arabidopsis. Planta 228, 411 425.
114. Cho Y-H, Yoo S-D Sheen J (2007) Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell 127, 579 585. (Pubitemid 351267580)
115. Balasubramanian R, Karve A, Kandasamy M, Meagher RB Moore BD (2007) A role for F-Actin in hexokinase-mediated glucose signaling. Plant Physiol 145, 1423 1434. (Pubitemid 350276762)
116. Chen JG (2007) Sweet sensor, surprising partners. Sci STKE 207, 1 4.
117. Stoltzman CA, Peterson CW, Breen KT, Muoio DM, Billin AN Ayer DE (2008) Glucose sensing by MondoA:Mlx complexes: a role for hexokinases and direct regulation of thioredoxin-interacting protein expression. Proc Natl Acad Sci U S A 105, 6912 6917.
118. Gancedo JM (2008) Early steps of glucose signaling in yeast. FEMS Microbiol Rev 32, 673 704.
119. Claeyssen E Rivoal J (2007) Isozymes of plant hexokinase: occurrence, properties and functions. Phytochemistry 68, 709 731. (Pubitemid 46330443)
120. Cho JI, Ryoo N, Eom JS, Lee DW, Kim HB, Jeong SW, Lee YH, Kwon YK, Cho MH, Bhoo SH et al. (2009) Role of the rice hexokinases OsHXK5 and OsHXK6 as glucose sensors. Plant Physiol 149, 745 759.
121. Pego JV Smeekens SC (2000) Plant fructokinases: a sweet family get-together. Trends Plant Sci 5, 531 536.
122. Rontein D, Dieuaide-Noubhani M, Dufourc EJ, Raymond P Rolin D (2002) The metabolic architecture of plant cells. Stability of central metabolism and flexibility of anabolic pathways during the growth cycle of tomato cells. J Biol Chem 277, 43948 43960. (Pubitemid 36157819)
123. Graham JW, Williams TC, Morgan M, Fernie AR, Ratclive RG Sweetlove LJ (2007) Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell 19, 3723 3738.
124. da-Silva WS, Gomez-Puyou A, de Gomez-Puyou MT, Moreno-Sanchez R, De Felice FG, de Meis L, Oliveira MF Galina A (2004) Mitochondrial bound hexokinase activity as a preventive antioxidant defense: steady-state ADP formation as a regulatory mechanism of membrane potential and reactive oxygen species generation in mitochondria. J Biol Chem 279, 39846 39855. (Pubitemid 39258256)
125. Arzoine L, Zilberberg N, Ben-Romano R Shoshan-Barmatz V (2009) Voltage-dependent anion channel 1-based peptides interact with hexokinase to prevent its anti-apoptotic activity. J Biol Chem 284, 3946 3955.
126. Abu-Hamad S, Arbel N, Calo D, Arzoine L, Israelson A, Keinan N, Ben-Romano R, Friedman O Shoshan-Barmatz V (2009) The VDAC1 N-terminus is essential both for apoptosis and the protective effect of anti-apoptotic proteins. J Cell Sci 122, 1906 1916.
127. Sun L, Shukair S, Naik TJ, Moazed F Ardehali H (2008) Glucose phosphorylation and mitochondrial binding are required for the protective effects of hexokinases I and II. Mol Cell Biol 28, 1007 1017. (Pubitemid 351160057)
128. Camacho-Pereira J, Meyer LE, Machado LB, Oliveira MF Galina A (2008) Reactive oxygen species production by potato tuber mitochondria is modulated by mitochondrially bound hexokinase activity. Plant Physiol 149, 1099 1110.
129. Dry IB, Nash D Wikisch JT (1983) The mitochondrial localization of hexokinase in pea leaves. Planta 158, 152 156.
130. Ehsani-Zonouz A, Golestani A Nemat-Gorgani M (2001) Interaction of hexokinase with the outer mitochondrial membrane and a hydrophobic matrix. Mol Cell Biochem 223, 81 87. (Pubitemid 32952093)
131. Goldin N, Arzoine L, Heyfets A, Israelson A, Zaslavsky Z, Bravman T, Bronner V, Notcovich A, Shoshan-Barmatz V Flescher E (2008) Methyl jasmonate binds to and detaches mitochondria-bound hexokinase. Oncogene 27, 4633 4635.
132. Zhang L Xing D (2008) Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death. Plant Cell Physiol 49, 1092 1111. (Pubitemid 351989697)
133. Linster CL, Adler LN, Webb K, Christensen KC, Brenner C Clarke SG (2008) A second GDP-L-galactose phosphorylase in Arabidopsis en route to vitamin C: covalent intermediate and substrate requirements for the conserved reaction. J Biol Chem 283, 18483 18492.
134. Conklin PL (2001) Recent advances in the role and biosynthesis of ascorbic acid in plants. Plant Cell Environ 24, 383 394.
135. Thomas CE, McLean LR, Parker RA Ohlweiler DF (1992) Ascorbate and phenolic antioxidant interactions in prevention of liposomal oxidation. Lipids 27, 543 550.
136. Bowles D, Lim EK, Poppenberger B Vaistij FE (2006) Glycosyltransferases of lipophilic small molecules. Annu Rev Plant Biol 57, 567 597. (Pubitemid 44061037)
137. Baroja-Fernandez E, Muñoz FJ, Montero M, Etxeberria E, Sesma MT, Ovecka M, Bahaji A, Ezquer I, Li J, Prat S et al. (2009) Enhancing sucrose synthase activity in transgenic potato (Solanum tuberosum L.) tubers results in increased levels of starch, ADPglucose and UDPglucose and total yield. Plant Cell Physiol 50, 1651 1662.
138. Inouhe M, Yamamoto R Masuda Y (2008) Inhibition of IAA-induced cell elongation in Avena coleoptile segments by galactose: its effect on UDP-glucose formation. Physiol Plant 66, 370 376.
139. Takahama U Oniki T (1997) A peroxide/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells. Plant Physiol 101, 845 852. (Pubitemid 28065368)
140. Neuhaus HE (2007) Transport of primary metabolites across the plant vacuolar membrane. FEBS Lett 581, 2223 2226.
141. Greutert H, Martinola E Keller F (1998) Mannitol transport by vacuoles of storage parenchyma of celery petioles operates by facilitated diffusion. J Plant Physiol 153, 91 96. (Pubitemid 28407774)
142. Klein M, Weisseboeck G, Dufaud A, Gaillard C, Kreuz K Martinoia E (1996) Different energization mechanisms drive the vacuolar uptake of a flavonoid glucoside and a herbicide glucoside. J Biol Chem 271, 29666 29671. (Pubitemid 26389591)
143. Goodman CD, Casati P Walbot V (2004) A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16, 1812 1826. (Pubitemid 38921303)
144. Lim PO Nam HG (2005) The molecular and genetic control of leaf senescence and longevity in Arabidopsis. Curr Top Dev Biol 67, 49 83.
145. Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T Pink D (2003) The molecular analysis of leaf senescence: a genomics approach. Plant Biotechnol J 1, 3 22.
146. Espinoza C, Vega A, Medina C, Schlauch K, Cramer G Arce-Johnson P (2007) Gene expression associated with compatible viral diseases in grapevine cultivars. Funct Integr Genomics 7, 95 110. (Pubitemid 46336166)
147. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin J-F, Wu S-H, Swidzinski J, Ishizaki K et al. (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signaling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42, 567 585. (Pubitemid 40722152)
148. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 9, 405 410. (Pubitemid 36726490)
149. Overmyer K, Brosché M Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8, 335 342. (Pubitemid 36996635)
150. Apel K Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55, 373 399. (Pubitemid 38940937)
151. Mittler R, Vanderauwera S, Gollery M Van Breusegem F (2004) Reactive oxygen network of plants. Trends Plant Sci 9, 490 498.
152. Foyer CH Noctor G (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28, 1056 1071. (Pubitemid 41577022)
153. Foyer CH Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866 1875.
154. Zhao Z, Chen G Zhang C (2001) Interaction between reactive oxygen species and nitric oxide in drought-induced abscisic acid synthesis in root tips of wheat seedlings. Aust J Plant Physiol 28, 1055 1061. (Pubitemid 33001825)
155. Xiong L, Schumaker KS Zhu J (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14, 165 183. (Pubitemid 36257495)
156. Chen C Dickman MB (2004) Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides. J Exp Bot 55, 2617 2623.
157. Laloi C, Apel K Danon A (2004) Reactive oxygen signaling: the latest news. Curr Opin Plant Biol 7, 323 328. (Pubitemid 38611053)
158. Wagner D, Przybyla D, Op den Camp R, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E et al. (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306, 1183 1185. (Pubitemid 39488997)
159. Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C Minibayeva F (2002) The apoplastic oxidative burst in response to biotic stress in 3 plants: a three-component system. J Exp Bot 53, 1367 1376. (Pubitemid 34544056)
160. 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)
161. Liu Y, Ren D, Pike S, Pallardy S, Gassmann W Zhang S (2007) Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J 51, 941 954. (Pubitemid 47376640)
162. Rhoads DM Subbaiah CC (2007) Mitochondrial retrograde regulation in plants. Mitochondrion 7, 177 194.
163. Prasad TK, Anderson MD, Martin BA Steward CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6, 65 74. (Pubitemid 2048331)
164. Wingler A Roitsch T (2008) Metabolic regulation of leaf senescence: interactions of sugar signaling with biotic and abiotic stress responses. Plant Biol 10, 50 62. (Pubitemid 352020108)
165. van Doorn WG (2008) Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels? J Exp Bot 59, 1963 1972.
166. Quirino BF, Noh YS, Himelblau E Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5, 278 282. (Pubitemid 30446034)
167. Dai N, Schaffer A, Petreikov M, Shahak Y, Giller Y, Ratner K, Levine A Granot D (1999) Overexpression of Arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis and induces rapid senescence. Plant Cell 11, 1253 1266.
168. Kim M, Lim JH, Ahn CS, Park K, Kim GT, Kim WT Pai HS (2006) Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. Plant Cell 18, 2341 2355. (Pubitemid 44484730)
169. Majewski N, Nogueira V, Bhaskar P, Coy PE, Skeen JE, Gottlob K, Chandel NS, Thompson CB, Robey RB Hay N (2004) Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol Cell 16, 819 830. (Pubitemid 39586539)
170. Stulke J Hillen W (1999) Carbon catabolite repression in bacteria. Curr Opin Microbiol 2, 195 201. (Pubitemid 29176945)
171. Brown V, Sabina F Johnston M (2009) Specialized sugar sensing in diverse fungi. Curr Biol 19, 436 441.
172. González JA, Reimann F Burdakov D (2009) Dissociation between sensing and metabolism of glucose in sugar sensing neurons. J Physiol 587, 41 48.