Trehalose and plant stress responses: Friend or foe?

Trends in Plant Science

Volumn 15, Issue 7, 2010, Pages 409-417

  Fernandez, Olivier ^a   Béthencourt, Linda ^b   Quero, Anthony ^b   Sangwan, Rajbir S ^b   Clement Christophe C ^a  

^a UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

^b UNIVERSITÉ DE PICARDIE JULES VERNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

TREHALOSE;

ANIMAL; APOPTOSIS; CHEMISTRY; CYTOLOGY; HUMAN; METABOLISM; MICROBIOLOGY; PHYSIOLOGICAL STRESS; PLANT; REVIEW; SYMBIOSIS;

ANIMALS; APOPTOSIS; HUMANS; PLANTS; STRESS, PHYSIOLOGICAL; SYMBIOSIS; TREHALOSE;

EID: 77955279908     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2010.04.004     Document Type: Review

References (86)

1. Richards A.B., et al. Trehalose: a review of properties, history of use and human tolerance, and results of multiple safety studies. Food Chem. Toxicol. 2002, 40:871-898.
2. Elbein A.D., et al. New insights on trehalose: a multifunctional molecule. Glycobiology 2003, 13:17-27.
3. Purvis J.E., et al. Enhanced trehalose production improves growth of Escherichia coli under osmotic stress. Appl. Environ. Microbiol. 2005, 71:3761-3769.
4. Cao Y., et al. Trehalose is an important mediator of Cap1p oxidative stress response in Candida albicans. Biol. Pharm. Bull. 2008, 31:421-425.
5. Ni M., Yu J.-H. A novel regulator couples sporogenesis and trehalose biogenesis in Aspergillus nidulans. PLoS ONE 2007, 2:e970.
6. Sakurai M., et al. Vitrification is essential for anhydrobiosis in an African chironomid. Polypedilum vanderplanki. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:5093-5098.
7. Paul M.J., et al. Trehalose metabolism and signaling. Annu. Rev. Plant Biol. 2008, 59:417-441.
8. Goddijn O.J.M., van Dun K. Trehalose metabolism in plants. Trends Plant Sci. 1999, 4:315-319.
9. Muller J., et al. Trehalose and trehalase in Arabidopsis. Plant Physiol. 2001, 125:1086-1093.
10. Garg A.K., et al. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15898-15903.
11. Karim S., et al. Improved drought tolerance without undesired side effects in transgenic plants producing trehalose. Plant Mol. Biol. 2007, 64:371-386.
12. Crowe J.H., et al. Trehalose as a " chemical chaperone": fact and fantasy. Adv. Exp. Med. Biol. 2007, 594:143-158.
13. Mahajan S., Tuteja N. Cold, salinity and drought stresses: an overview. Arch. Biochem. Biophys. 2005, 444:139-158.
14. Plant Pathology 2005, Academic Press, Elsevier. G.N. Agrios (Ed.).
15. Plant Responses to Abiotic Stress 2004, Springer. H. Hirt, K. Shinozaki (Eds.).
16. Chinnusamy V., et al. Cold stress regulation of gene expression in plants. Trends Plant Sci. 2007, 12:444-451.
17. Zhao S., Qi X. Signaling in plant disease resistance and symbiosis. J. Integr. Plant Biol. 2008, 50:799-807.
18. Bari R., Jones J. Role of plant hormones in plant defence responses. Plant Mol. Biol. 2009, 69:473-488.
19. van Loon L.C., et al. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 2006, 44:135-162.
20. Moore J.P., et al. Towards a systems-based understanding of plant desiccation tolerance. Trends Plant Sci. 2009, 14:110-117.
21. Hammerschmidt R. Phytoalexins: what have we learned after 60 years?. Annu. Rev. Phytopathol. 1999, 37:285-306.
22. Veyres N., et al. The Arabidopsis sweetie mutant is affected in carbohydrate metabolism and defective in the control of growth, development and senescence. Plant J. 2008, 55:665-686.
23. Avonce N., et al. Insights on the evolution of trehalose biosynthesis. BMC Evol. Biol. 2006, 6:109-113.
24. Jules M., et al. New insights into trehalose metabolism by Saccharomyces cerevisiae: NTH2 encodes a functional cytosolic trehalase, and deletion of TPS1 reveals Ath1p-dependent trehalose mobilization. Appl. Environ. Microbiol. 2008, 74:605-614.
25. Blázquez M.A., et al. Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase. Plant J. 1998, 13:685-689.
26. Vogel G., et al. Trehalose-6-phosphate phosphatases from Arabidopsis thaliana: identification by functional complementation of the yeast tps2 mutant. Plant J. 1998, 13:673-683.
27. Leyman B., et al. An unexpected plethora of trehalose biosynthesis genes in Arabidopsis thaliana. Trends Plant Sci. 2001, 6:510-513.
28. Frison M., et al. The Arabidopsis thaliana trehalase is a plasma membrane-bound enzyme with extracellular activity. FEBS Lett. 2007, 581:4010-4016.
29. Liu M., et al. Constitutive components and induced gene expression are involved in the desiccation tolerance of Selaginella tamariscina. Plant Cell Physiol. 2008, 49:653-663.
30. Drennan P.M., et al. The occurence of trehalose in the leaves of the desiccation-tolerant angiosperm Myrothamnus flabellifolius welw. J. Plant. Physiol. 1993, 142:493.
31. Kaplan F., et al. Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol. 2004, 136:4159-4168.
32. Kosmas S., et al. Isolation and characterization of drought-related trehalose 6-phosphate-synthase gene from cultivated cotton (Gossypium hirsutum L.). Planta 2006, 223:329-339.
33. Zhuang Y., et al. Effects of water-deficit stress on the transcriptomes of developing immature ear and tassel in maize. Plant Cell Rep. 2007, 26:2137-2147.
34. Pramanik M.H.R., Imai R. Functional identification of a trehalose 6-phosphate phosphatase gene that is involved in transient induction of trehalose biosynthesis during chilling stress in rice. Plant Mol. Biol. 2005, 58:751-762.
35. Shima S., et al. Biochemical characterization of rice trehalose-6-phosphate phosphatases supports distinctive functions of these plant enzymes. FEBS J. 2007, 274:1192-1201.
36. López M., et al. Trehalose and trehalase in root nodules of Medicago truncatula and Phaseolus vulgaris in response to salt stress. Physiol. Plant. 2008, 134:575-582.
37. Iordachescu M., Imai R. Trehalose biosynthesis in response to abiotic stresses. J. Integr. Plant Biol. 2008, 50:1223-1229.
38. Garcia A.B., et al. Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol. 1997, 115:159-169.
39. Bae H., et al. Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification, abiotic stress, nitrogen metabolism, and plant defense. Physiol. Plant. 2005, 125:114-126.
40. Bae H., et al. Exogenous trehalose promotes non-structural carbohydrate accumulation and induces chemical detoxification and stress response proteins in Arabidopsis thaliana grown in liquid culture. Plant Sci. 2005, 168:1293-1301.
41. Romero C., et al. Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta 1997, 201:293-297.
42. Avonce N., et al. The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol. 2004, 136:3649-3659.
43. Cortina C., Culianez-Macia F.A. Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci. 2005, 169:75-82.
44. Miranda J., et al. A bifunctional TPS-TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta 2007, 226:1411-1421.
45. Ramon M., et al. ABI4 mediates the effects of exogenous trehalose on Arabidopsis growth and starch breakdown. Plant Mol. Biol. 2007, 63:195-206.
46. Schluepmann H., et al. Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiol. 2004, 135:879-890.
47. Fujita M., et al. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 2006, 9:436-442.
48. Mithöfer A. Suppression of plant defence in rhizobia-legume symbiosis. Trends Plant Sci. 2002, 7:440-444.
49. Streeter J.G., Gomez M.L. Three enzymes for trehalose synthesis in Bradyrhizobium cultured bacteria and in bacteroids from soybean nodules. Appl. Environ. Microbiol. 2006, 72:4250-4255.
50. Farias-Rodriguez R., et al. The accumulation of trehalose in nodules of several cultivars of common bean (Phaseolus vulgaris) and its correlation with resistance to drought stress. Physiol. Plant. 1998, 102:353-359.
51. Suárez R., et al. Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol. Plant Microbe Interact. 2008, 21:958-966.
52. Ampomah O.Y., et al. Lack of trehalose catabolism in Sinorhizobium species increases their nodulation competitiveness on certain host genotypes. New Phytol. 2008, 179:495-504.
53. Nehls U. Mastering ectomycorrhizal symbiosis: the impact of carbohydrates. J. Exp. Bot. 2008, 59:1097-1108.
54. López M.F., et al. Increased trehalose biosynthesis in Hartig net hyphae of ectomycorrhizas. New Phytol. 2007, 174:389-398.
55. Renard-Merlier D., et al. Iodus 40, salicylic acid, heptanoyl salicylic acid and trehalose exhibit different efficacies and defence targets during a wheat/powdery mildew interaction. Phytochemistry 2007, 68:1156-1164.
56. Muchembled J., et al. Changes in lipid composition of Blumeria graminis f. sp. tritici conidia produced on wheat leaves treated with heptanoyl salicylic acid. Phytochemistry 2006, 67:1104-1109.
57. Brodmann D., et al. Induction of trehalase in Arabidopsis plants infected with the trehalose-producing pathogen Plasmodiophora brassicae. Mol. Plant Microbe Interact. 2002, 15:693-700.
58. Isidorov V., et al. Gas chromatographic-mass spectrometric investigation of metabolites from the needles and roots of pine seedlings at early stages of pathogenic fungi Armillaria ostoyae attack. Trees 2008, 22:531-542.
59. Gancedo C., Flores C.L. The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Res. 2004, 4:351-359.
60. Foster A.J., et al. Trehalose synthesis and metabolism are required at different stages of plant infection by Magnaporthe grisea. EMBO J. 2003, 22:225-235.
61. Wilson R.A., et al. Tps1 regulates the pentose phosphate pathway, nitrogen metabolism and fungal virulence. EMBO J. 2007, 26:3673-3685.
62. Gibon Y., et al. Is glycine betaine a non-compatible solute in higher plants that do not accumulate it?. Plant Cell Environ. 1997, 20:329-340.
63. Gagneul D., et al. A reassessment of the function of the so-called compatible solutes in the halophytic Plumbaginaceae Limonium latifolium. Plant Physiol. 2007, 144:1598-1611.
64. Schluepmann H., et al. Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:6849-6854.
65. Grennan A.K. The role of trehalose biosynthesis in plants. Plant Physiol. 2007, 144:3-5.
66. El-Bashiti T., et al. Biochemical analysis of trehalose and its metabolizing enzymes in wheat under abiotic stress conditions. Plant Sci. 2005, 169:47-54.
67. Miller G., et al. Reactive oxygen signaling and abiotic stress. Physiol. Plant. 2008, 133:481-489.
68. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002, 7:405-410.
69. Luo Y., et al. Trehalose: protector of antioxidant enzymes or reactive oxygen species scavenger under heat stress?. Environ. Exp. Bot. 2008, 63:378-384.
70. da Costa Morato Nery D., et al. The role of trehalose and its transporter in protection against reactive oxygen species. Biochim. Biophys. Acta 2008, 1780:1408-1411.
71. Reape T.J., McCabe P.F. Apoptotic-like programmed cell death in plants. New Phytol. 2008, 180:13-26.
72. del Pozo O., Lam E. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr. Biol. 1998, 8:1129-1132.
73. Danon A., et al. Ultraviolet-C overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and defender against apoptotic death. J. Biol. Chem. 2004, 279:779-787.
74. Qi L., et al. Trehalose inhibited the phagocytosis of refrigerated platelets in vitro via preventing apoptosis. Transfusion 2009, 49:2158-2166.
75. Sasnoor L.M., et al. Prevention of apoptosis as a possible mechanism behind improved cryoprotection of hematopoietic cells by catalase and trehalose. Transplantation 2005, 80:1251-1260.
76. Yamada T., et al. Suppressive effect of trehalose on apoptotic cell death leading to petal senescence in ethylene-insensitive flowers of gladiolus. Plant Sci. 2003, 164:213-221.
77. Hruz T., et al. Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinformatics 2008, 2008:420747.
78. Jones J.D.G., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
79. Hanson J., Smeekens S. Sugar perception and signaling - an update. Curr. Opin. Plant Biol. 2009, 12:562-567.
80. Rolland F., et al. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 2006, 57:675-709.
81. Pereira C.S., et al. Interaction of the disaccharide trehalose with a phospholipid bilayer: a molecular dynamics study. Biophys. J. 2004, 86:2273-2285.
82. Lunn J.E., et al. 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. 2006, 397:139-148.
83. Zhang Y., et al. Inhibition of SNF1-Related Protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol. 2009, 149:1860-1871.
84. Paul M.J., et al. Upregulation of biosynthetic processes associated with growth by trehalose 6-phosphate. Plant Signal. Behav. 2010, 5:386-392.
85. Harthill J.E., et al. Phosphorylation and 14-3-3 binding of Arabidopsis trehalose-phosphate synthase 5 in response to 2-deoxyglucose. Plant J. 2006, 47:211-223.
86. Pitzschke A., et al. MAPK cascade signalling networks in plant defence. Curr. Opin. Plant Biol. 2009, 12:421-426.