Exogenous trehalose largely alleviates ionic unbalance, ROS burst, and PCD occurrence induced by high salinity in arabidopsis seedlings

Frontiers in Plant Science

Volumn 5, Issue October, 2014, Pages

  Yang, Lei ^a   Zhao, Xiaoju ^b   Zhu, Hong ^c   Paul, Matthew ^d   Zu, Yuangang ^c   Tang, Zhonghua ^c  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b DAQING NORMAL UNIVERSITY   (China)

^c NORTHEAST FORESTRY UNIVERSITY   (China)

^d ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

Arabidopsis; Ion homeostasis; Redox state; Salt stress; Trehalose

Indexed keywords

EID: 84908360583     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00570     Document Type: Article

References (54)

1. Affenzeller, M. J., Darehshouri, A., Andosch, A., Lutz, C., and Lutz-Meindl, U. (2009). Salt stress-induced cell death in the unicellular green alga Micrasterias denticulata. J. Exp. Bot. 60, 939-954. doi: 10.1093/jxb/ern348.
2. Arguelles, J. C. (2000). Physiological roles of trehalose in bacteria and yeasts: a comparativeanalysis. Arch. Microbiol. 174,217-224. doi: 10.1007/s002030000192.
3. Avonce, N., Leyman, B., Mascorro-Gallardo, J. O., Van Dijck, P., Thevelein, J. M., and Iturriaga, G. (2004). The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol. 136, 3649-3659. doi: 10.1104/pp.104.052084.
4. Bae, H., Herman, E., Bailey, B., Bae, H.-J., and Sicher, R. (2005). Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification, abiotic stress, nitrogen metabolism, and plant defense. Physiol. Plant. 125,114-126. doi: 10.1111/j.1399-3054.2005.00537.x
5. Beauchamp, C., and Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44, 276-287. doi: 10.1016/0003-2697(71)90370-8.
6. Chang, B., Yang, L., Cong, W., Zu, Y., and Tang, Z.(2014). The improved resistance to high salinity induced by trehalose is associated with ionic regulation and osmotic adjustment in Catharanthus roseus. Plant Physiol. Biochem. 77, 140-148. doi: 10.1016/j.plaphy.2014.02.001.
7. Cuin, T. A., and Shabala, S. (2007). Compatible solutes reduce ROS-induced potassium efflux in Arabidopsis roots. Plant Cell Environ. 30, 875-885. doi: 10.1111/j.1365-3040.2007.01674.x
8. Elbein, A. D., Pan, Y. T., Pastuszak, I., and Carroll, D. (2003). New insights on trehalose: a multifunctional molecule. Glycobiology 13, 17R-27R. doi: 10.1093/glycob/cwg047.
9. Eleutherio, E. C., Araujo, P. S., and Panek, A. D. (1993). Protective role of trehalose during heat stress in Saccharomyces cerevisiae. Cryobiology 30, 591-596. doi: 10.1006/cryo.1993.1061.
10. Fernandez, O., Bethencourt, L., Quero, A., Sangwan, R. S., and Clement, C. (2010). Trehalose and plant stress responses: friend or foe? Trends Plant Sci. 15,409-417. doi: 10.1016/j.tplants.2010.04.004.
11. Garcia, A. B., Engler, J., Iyer, S., Gerats, T., Van Montagu, M., and Caplan, A. B. (1997). Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol. 115, 159-169.
12. Garg, A. K., Kim, J. K., Owens, T. G., Ranwala, A. P., Choi, Y. D., Kochian, L. V., et al. (2002). Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc. Natl. Acad. Sci. U.S.A. 99, 15898-15903. doi: 10.1073/pnas.252637799.
13. Ge, L. F., Chao, D. Y., Shi, M., Zhu, M. Z., Gao, J. P., and Lin, H. X. (2008). Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 228, 191-201.doi: 10.1007/s00425-008-0729-x
14. Genc, Y., McDonald, G. K., and Tester, M. (2007). Reassessment of tissue Na+ concentration as a criterion for salinity tolerance in bread wheat. Plant Cell Environ. 30, 1486-1498. doi: 10.1111/j.1365-3040.2007.01726.x
15. Halweg, C., Thompson, W. F., and Spiker, S. (2005). The rb7 matrix attachment region increases the likelihood and magnitude oftransgene expression in tobacco cells:aflowcytometric study. PlantCell 17,418-429. doi: 10.1105/tpc.104.028100.
16. Harrach, B., Fodor, J., Pogany, M., Preuss, J., and Barna, B. (2008). Antioxidant, ethylene and membrane leakage responses to powdery mildew infection of near-isogenic barley lines with various types of resistance. Eur. J. Plant Pathol. 121, 21-33. doi: 10.1007/s10658-007-9236-3.
17. Hasegawa, P. M., Bressan, R. A., Zhu, J. K., and Bohnert, H. J. (2000). Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51,463-499. doi: 10.1146/annurev.arplant.51.1.463.
18. Higo, A., Katoh, H., Ohmori, K., Ikeuchi, M., and Ohmori, M. (2006). The role of a gene cluster for trehalose metabolism in dehydration tolerance of the filamentous cyanobacterium Anabaena sp. PCC 7120. Microbiology 152, 979-987. doi: 10.1099/mic.0.28583-0.
19. Hoeberichts, F. A., and Woltering, E. J. (2003). Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators. Bioessays 25, 47-57. doi: 10.1002/bies.10175.
20. Iordachescu, M., and Imai, R. (2008). Trehalose biosynthesis in response to abiotic stresses. J. Integr. Plant Biol. 50, 1223-1229. doi: 10.1111/j.1744-7909.2008.00736.x
21. Jiang, A. L., Cheng, Y., Li, J., and Zhang, W. (2008). A zinc-dependent nuclear endonuclease is responsible for DNA laddering during salt-induced programmed cell death in root tip cells of rice. J. Plant Physiol. 165, 1134-1141. doi: 10.1016/j.jplph.2007.12.008.
22. Jiang, C., Belfield, E. J., Cao, Y., Smith, J. A., and Harberd, N. P. (2013). An Arabidopsis soil-salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis. Plant Cell 25, 3535-3552. doi: 10.1105/tpc.113.115659.
23. Jorge, J. A., Polizeli, M. L., Thevelein, J. M., and Terenzi, H. F. (1997). Treha-lases and trehalose hydrolysis in fungi. FEMS Microbiol. Lett. 154, 165-171. doi: 10.1111/j.1574-6968.1997.tb12639.x
24. Karim, S., Aronsson, H., Ericson, H., Pirhonen, M., Leyman, B., Welin, B., etal. (2007). Improved drought tolerance without undesired side effects in transgenic plants producing trehalose. Plant Mol. Biol. 64, 371-386. doi: 10.1007/s11103-007-9159-6
25. Li, H. W., Zang, B. S., Deng, X. W., and Wang, X. P. (2011). Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234, 1007-1018.doi: 10.1007/s00425-011-1458-0.
26. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193,265-275.
27. Lunn, J. E., Delorge, I., Figueroa, C. M., Van Dijck, P., and Stitt, M. (2014). Trehalose metabolism in plants. Plant J. 79, 544-567. doi: 10.1111/tpj.12509.
28. Lunn, J. E., Feil, R., Hendriks, J. H., Gibon, Y., Morcuende, R., Osuna, D., etal. (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. doi: 10.1042/BJ20060083
29. Luo, Y., Li, W.-M., and Wang, W. (2008). Trehalose: protector ofantioxidant enzymes or reactive oxygen species scavenger under heat stress? Environ. Exp. Bot. 63, 378-384. doi: 10.1016/j.envexpbot.2007.11.016.
30. Miller, G., Shulaev, V., and Mittler, R. (2008). Reactive oxygen signaling and abiotic stress. Physiol. Plant. 133,481-489. doi: 10.1111/j.1399-3054.2008.01090.x
31. Mittler, R., Vanderauwera, S., Gollery, M., and Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498. doi: 10.1016/j.tplants.2004.08.009.
32. Mittova, V., Guy, M., Tal, M., and Volokita, M. (2004). Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J. Exp. Bot. 55, 1105-1113. doi: 10.1093/jxb/erh113
33. Moon, H., Lee, B., Choi, G., Shin, D., Prasad, D. T., Lee, O., et al. (2003). NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc. Natl. Acad. Sci. U.S.A. 100,358-363. doi: 10.1073/pnas.252641899.
34. Munns, R. (2002). Comparative physiology of salt and water stress. Plant Cell Environ. 25,239-250. doi: 10.1046/j.0016-8025.2001.00808.x
35. Munns, R., and Tester, M. (2008). Mechanisms of salinity tolerance. Annu. Rev. PlantBiol. 59, 651-681. doi: 10.1146/annurev.arplant.59.032607.092911.
36. Patterson, B. D., Payne, L. A., Chen, Y. Z., and Graham, D. (1984). An inhibitor of catalase induced by cold in chilling-sensitive plants. PlantPhysiol. 76,1014-1018. doi: 10.1104/pp.76.4.1014.
37. Paul, A., Hauck, M., and Fritz, E. (2003). Effects of manganese on element distribution and structure in thalli of the epiphytic lichens Hypogymnia physodes and Lecanora conizaeoides. Environ. Exp. Bot. 50, 113-124. doi: 10.1016/S0098-8472(03)00017-0.
38. Paul, M. J., Jhurreea, D., Zhang, Y., Primavesi, L. F., Delatte, T., Schluep-mann, H., etal. (2010). Upregulation of biosynthetic processes associated with growth by trehalose 6-phosphate. Plant Signal. Behav. 5, 386-392. doi: 10.4161/psb.5.4.10792.
39. Paul, M. J., Primavesi, L. F., Jhurreea, D., and Zhang, Y. (2008). Trehalose metabolism and signaling. Annu. Rev. Plant Biol. 59, 417-441. doi: 10.1146/annurev.arplant.59.032607.092945.
40. Penna, S. (2003). Building stress tolerance through over-producing trehalose in transgenic plants. Trends Plant Sci. 8, 355-357. doi: 10.1016/S1360-1385(03)00159-6
41. Rathmell, W. G., and Sequeira, L. (1974). Soluble peroxidase in fluid from the intercellular spaces of tobacco leaves. Plant Physiol. 53, 317-318. doi: 10.1104/pp.53.2.317
42. Rus, A., Yokoi, S., Sharkhuu, A., Reddy, M., Lee, B.-H., Matsumoto, T. K., etal. (2001). AtHKT1isa salt tolerance determinant that controls Na+ entry into plant roots. Proc. Natl. Acad. Sci. U.S.A. 98,14150-14155. doi: 10.1073/pnas.241501798.
43. Schluepmann, H., Berke, L., and Sanchez-Perez, G. F. (2012). Metabolism control over growth:acasefortrehalose-6-phosphateinplants. J. Exp. Bot. 63,3379-3390. doi: 10.1093/jxb/err311.
44. Schluepmann, H., Pellny, T., van Dijken, A., Smeekens, S., and Paul, M. (2003). Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 100, 6849-6854. doi: 10.1073/pnas.1132018100.
45. Shabala, S. (2009). Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J. Exp. Bot. 60, 709-712. doi: 10.1093/jxb/erp013.
46. Tang, Z. H., Liu, Y. J., Guo, X. R., and Zu, Y. G. (2011). The combined effects of salinity and nitrogen forms on Catharanthus roseus: the role of internal ammonium and free amino acids during salt stress. J. PlantNutr. Soil Sci. 174,135-144. doi: 10.1002/jpln.200900354.
47. Vranova, E., Inze, D., and Van Breusegem, F. (2002). Signal transduction during oxidative stress. J. Exp. Bot. 53,1227-1236. doi: 10.1093/jexbot/53.372.1227.
48. Wiemken, A. (1990). Trehalose in yeast, stress protectant rather than reserve carbohydrate. Antonie Van Leeuwenhoek 58, 209-217. doi: 10.1007/BF00548935.
49. Wingler, A., Delatte, T. L., O’Hara, L. E., Primavesi, L. F., Jhurreea, D., Paul, M. J., etal. (2012). Trehalose 6-phosphate is required for the onset of leaf senes-cenceassociatedwithhighcarbonavailability. PlantPhysiol. 158,1241-1251. doi: 10.1104/pp.111.191908.
50. Wingler, A., Fritzius, T., Wiemken, A., Boller, T., and Aeschbacher, R. A. (2000). Trehalose induces the ADP-glucose pyrophosphorylase gene, ApL3, and starch synthesisin Arabidopsis. PlantPhysiol. 124, 105-114. doi: 10.1104/pp.124.1.105.
51. Yamada, T., Takatsu, Y., Manabe, T., Kasumi, M., and Marubashi, W. (2003). Suppressive effect of trehalose on apoptotic cell death leading to petal senescence in ethylene-insensitive flowers of gladiolus. Plant Sci. 164, 213-221. doi: 10.1016/S0168-9452(02)00403-X
52. Yang, L., Zu, Y. G., and Tang, Z. H. (2013). Ethylene improves Arabidopsis salt tolerance mainlyviaretaining K+ in shoots and roots rather than decreasing tissue Na+ content. Environ. Exp. Bot. 86, 60-69. doi: 10.1016/j.envexpbot.2010.08.006.
53. Zhu, J. K. (2001). Plantsalttolerance. TrendsPlantSci. 6,66-71. doi: 10.1016/S1360-1385(00)01838-0
54. Zhu, J. K., Liu, J., and Xiong, L. (1998). Genetic analysis ofsalt tolerancein Arabidop-sis. Evidence for a critical role of potassium nutrition. Plant Cell 10, 1181-1191. doi: 10.1105/tpc.10.7.1181