Neutral invertase, hexokinase and mitochondrial ROS homeostasis: Emerging links between sugar metabolism, sugar signaling and ascorbate synthesis

Plant Signaling and Behavior

Volumn 6, Issue 10, 2011, Pages 1567-1573

  Xiang, Li ^a   Li, Yi ^b   Rolland, Filip ^b   van den Ende, Wim ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b Functional Biology   (Belgium)

Author keywords

Ascorbate peroxidase; Glucose; Hexokinase; Mitochondria; Neutral invertase; Oxidative stress; Sucrose

Indexed keywords

ARABIDOPSIS; PHOTOBACTERIA;

EID: 80053623967     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.6.10.17036     Document Type: Article

References (50)

1. Vargas WA, Pontis HG, Salerno GL. New insights on sucrose metabolism: evidence for an active A/N Inv in chloroplasts uncovers a novel component of the intracellular carbon trafficking. Planta 2008; 227:795-807.
2. Murayama S, Handa H. Genes for alkaline/neutral invertase in rice: alkaline/neutral invertases are located in plant mitochondria and also in plastids. Planta 2007; 225:1193-203.
3. Vargas WA, Pontis HG, Salerno GL. Differential expression of alkaline and neutral invertases in response to environmental stresses: characterization of an alkaline isoform as a stress-response enzyme in wheat leaves. Planta 2007; 226:1535-45.
4. Vargas WA, Salerno GL. The Cinderella story of sucrose hydrolysis: Alkaline/neutral invertases, from cyanobacteria to unforeseen roles in plant cytosol and organelles. Plant Sci 2010; 178:1-8.
5. Van den Ende W, Van Laere A. Purification and properties of a neutral invertase from the roots of Cichorium intybus L. Physiol Plant 1995; 93:241-8.
6. Barratt DHP, Derbyshire P, Findlay K, Pike M, Wellner N, Lunn J, et al. Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase. Proc Natl Acad Sci USA 2009; 106:13124-9.
7. Welham T, Pike J, Horst I, Flemetakis E, Katinakis P, Kaneko T, et al. A cytosolic invertase is required for normal growth and cell development in the model legume, Lotus japonicus. J Exp Bot 2009; 60:3353-65.
8. Lou Y, Gou JY, Xue HW. PIP5K9, an Arabidopsis phosphatidylinositol monophosphate kinase, interacts with a cytosolic invertase to negatively regulate sugar mediated root growth. Plant Cell 2007; 19:163-81.
9. Qi X, Wu Z, Li J, Mo X, Wu S, Chu J, et al. AtCYTINV1, a neutral invertase, is involved in osmotic stress-induced inhibition on lateral root growth in Arabidopsis. Plant Mol Biol 2007; 64:575-87.
10. Jia L, Zhang B, Mao C, Li J, Wu Y, Wu P, Wu Z. OsCYT-INV1 for alkaline/neutral invertase is involved in root cell development and reproductivity in rice (Oryza sativa L.). Planta 2008; 288:51-9.
11. Yao SG, Kodama R, Wang H, Ichii M, Taketa S, Yoshida H. Analysis of the rice SHORT-ROOT5 gene revealed functional diversification of plant neutral/alkaline invertase family. Plant Sci 2009; 176:627-34.
12. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 2003; 422:442-6.
13. Pnueli L, Liang H, Rozenberg M, Mittler R. Growth suppression, altered stomatal responses and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J 2003; 34:187-203.
14. Rizhsky L, Liang H, Mittler R. The water-water cycle is essential for chloroplast protection in the absence of stress. J Biol Chem 2003; 278:38921-5.
15. Sulmon C, Gouesbet G, El Amrani A, Couée I. Sugar-induced tolerance to the herbicide atrazine in Arabidopsis seedlings involves activation of oxidative and xenobiotic stress responses. Plant Cell Rep 2006; 25:489-98.
16. Nishizawa A, Yukinori Y, Shigeoka S. Galactinol and raffinose as a novel function to protect plants from oxidative damage. Plant Physiol 2008; 147:1251-63.
17. Ramel F, Sulmon C, Bogard M, Couée I, Gouesbet G. Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biol 2009; 9:28-45.
18. Camacho-Pereira J, Meyer LE, Machado LB, Oliveira MF, Galina A. Reactive oxygen species production by potato tuber mitochondria is modulated by mitochondrially bound hexokinase activity. Plant Physiol 2009; 149:1099-100.
19. Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W. Sugar signaling and antioxidant network connections in plant cells. FEBS J 2010; 277:2022-37.
20. Rolland F, Baena-Gonzalez E, Sheen J. Sugar sensing and signaling in plants: Conserved and novel mechanisms. Ann Rev Plant Biol 2006; 57:675-709.
21. Li Y, Smith C, Corke F, Zheng L, Merali Z, Ryden P, et al. Signaling from an altered cell wall to the nucleus mediates sugar-responsive growth and development in Arabidopsis thaliana. Plant Cell 2007; 19:2500-15.
22. Noctor G, Foyer CH. A re-evaluation of the ATP:NADPH budget during C3 photosynthesis. A contribution from nitrate assimilation and its associated respiratory activity? J Exp Bot 1998; 49:1895-2008.
23. Maruta T, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, et al. Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol 2010; 51:190-200.
24. Mittova V, Guy M, Tal M, Volokita M. Salinity upregulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 2004; 55:1105-13.
25. Chang CCC, Ball L, Fryer MJ, Baker NR, Karpinski S, Mullineaux PM. Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signaling pathways but is associated with changes in photosynthesis. Plant J 2004; 38:499-511.
26. Graham JWA, Williams TCR, Morgan M, Fernie AR, Ratcliffe RG, Sweetlove LJ. Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell 2007; 19:3723-38.
27. Szarka A, Horemans N, Passarella S, Tarcsay A, Orsi F, Salgó A, et al. Demonstration of an intramitochondrial invertase activity and the corresponding sugar transporters of the inner mitochondrial membrane in Jerusalem artichoke (Helianthus tuberosus L.) tubers. Planta 2008; 228:765-75.
28. Goldin N, Arzoine L, Heyfets A, Israelson A, Zaslavsky Z, Bravman T. Methyl jasmonate binds to and detaches mitochondria-bound hexokinase. Oncogene 2008; 27:4636-43.
29. Jubany-Mari T, Prinsen E, Munne-Bosch S, Alegre L. The timing of methyl jasmonate, hydrogen peroxide and ascorbate accumulation during water deficit and subsequent recovery in the Mediterranean shrub Cistus albidus L. Env Exp Bot 2010; 69:47-55.
30. Soares A, de Souza TF, Domingues S, Jacinto T, Machado OLT. Methyl jasmonate promotes the transient reduction of the levels of 2-Cys peroxiredoxin in Ricinus communis plants. Plant Physiol Biochem 2004; 42:543-7.
31. Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N. Coordinated activation of metabolic pathways for antioxidants and defense compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 2005; 44:653-68.
32. Wolucka BA, Goossens A, Inze D. Methyl jasmonate stimulates the de novo biosynthesis of vitamin C in plant cell suspensions. J Exp Bot 2005; 56:2527-38.
33. Xiang CB, Oliver DJ. Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 1998; 10:1539-50.
34. Shan CJ, Liang ZS. Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Plant Sci 2010; 178:130-9.
35. Ju FW, Koh EJ, Kim SH, Kim KI, Lee H, Hong SW. Glucosamine causes overproduction of reactive oxygen species, leading to repression of hypocotyl elongation through a hexokinase-mediated mechanism in Arabidopsis. J Plant Physiol 2009; 166:203-12.
36. Wachter A, Wolf S, Steininger H, Bogs J, Rausch T. Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. Plant J 2005; 41:15-30.
37. Linster CL, Clarke SG. L-Ascorbate biosynthesis in higher plants: the role of VTC2. Trends Plant Sci 2008; 13:567-73.
38. Davey MW, Gilot C, Persiau G, Ostergaard J, Han Y, Bauw GC. Ascorbate biosynthesis in Arabidopsis cell suspension culture. Plant Physiol 1999; 121:535-43.
39. Lorence A, Chevone BI, Mendes P, Nessler CL. Myo-inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiol 2004; 134:1200-5.
40. Maruta T, Ichikawa Y, Mieda T, Takeda T, Tamoi M, Yabuta Y. The contribution of Arabidopsis homologs of L-gulono-1,4-lactone oxidase to the biosynthesis of ascorbic acid. Biosci Biotech Biochem 2010; 74:1494-7.
41. Zhang YH, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RAC, Powers SJ. Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 2009; 149:1860-71.
42. Ma J, Hanssen M, Lundgren K, Hernández L, Delatte T, Ehlert A, et al. The sucrose-regulated Arabidopsis transcription factor bZIP11 reprograms metabolism and regulates trehalose metabolism. New Phytol 2011; 191:733-45.
43. Ananieva EA, Gillaspy GE, Ely A, Burnette RN, Erickson FL. Interaction of the WD40 domain of a myoinositol polyphosphate-5-phosphatase with SnRK1 links inositol, sugar and stress signaling. Plant Physiol 2008; 148:1868-82.
44. Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J. A central integrator of transcription networks in plant stress and energy signaling. Nature 2007; 448:938-42.
45. Gibon Y, Usadel B, Blaesing OE, Kamlage B, Hoehne M, Trethewey R. Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biol 2006; 7:76.
46. Price J, Laxmi A, St-Martin SK, Jang JC. Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 2004; 16:2128-50.
47. Ananieva EA, Gillaspy GE. Switches in nutrient and inositol signaling. Plant Signal Behav 2009; 4:304-6.
48. Armengaud P, Breitling R, Amtmann A. The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 2004; 136:2556-76.
49. Foyer CH, Noctor G. Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 2011; 155:2-18.
50. Li MJ, Ma FW, Liu J, Li JA. Shading the whole vines during young fruit development decreases ascorbate accumulation in kiwi. Physiol Plant 2010; 140:225-37