Development of salinity tolerance in rice by constitutive-overexpression of genes involved in the regulation of programmed cell death

Frontiers in Plant Science

Volumn 6, Issue , 2015, Pages

  Hoang, Thi M L ^a   Moghaddam, Lalehvash ^a   Williams, Brett ^a   Khanna, Harjeet ^b   Dale, James ^a   Mundree, Sagadevan G ^a  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b BSES LIMITED   (Australia)

Author keywords

Abiotic stress; Anti apoptotic; Apoptosis; Programmed cell death; Rice; ROS; Salinity stress; TUNEL

Indexed keywords

EID: 84942905635     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00175     Document Type: Article

References (79)

1. Apel, K., and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399. doi: 10.1146/annurev.arplant.55.031903.141701
2. Ashraf, M. (2004). Some important physiological selection criteria for salt tolerance in plants. Flora Morphol. Distribution, Funct. Ecol. Plants 199, 361–376. doi: 10.1078/0367-2530-00165
3. Ashraf, M., Athar, H. R., Harris, P. J. C., and Kwon, T. R. (2008). “Some prospective strategies for improving crop salt tolerance,” in Advances in Agronomy, ed. L. S. Donald (Waltham, MA: Academic Press), 45–110.
4. Barth, A. (2000). The infrared absorption of amino acid side chains. Prog. Biophys. Mol. Biol. 74, 141–173. doi: 10.1016/S0079-6107(00)00021-3
5. Bertin, J., Mendrysa, S. M., Lacount, D. J., Gaur, S., Krebs, J. F., Armstrong, R. C., et al. (1996). Apoptotic suppression by baculovirus P35 involves cleavage by and inhibition of a virus-induced CED-3/ICE-like protease. J. Virol. 70, 6251–6259.
6. Bhatnagar-Mathur, P., Vadez, V., and Sharma, K. K. (2008). Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep. 27, 411–424. doi: 10.1007/s00299-007-0474-479
7. Bhattacharjee, S. (2012). The language of reactive oxygen species signaling in plants. J. Bot. 2012, 22. doi: 10.1155/2012/985298
8. Blumwald, E. (2000). Sodium transport and salt tolerance in plants. Curr. Opin. Cell Biol. 12, 431–434. doi: 10.1016/S0955-0674(00)00112-5
9. Borsani, O., Zhu, J., Verslues, P. E., Sunkar, R., and Zhu, J.-K. (2005). Endogenous sirnas derived from a pair of natural cis-antisense transcripts regulate salt tolerance in arabidopsis. Cell 123, 1279–1291. doi: 10.1016/j.cell.2005. 11.035
10. Brodsky, J. L., and Bracher, A. (2007). “Nucleotide exchange factors for Hsp70 molecular chaperones,” in Networking of Chaperones by Co-Chaperones, ed. G. L. Blatch (New York: Landes Bioscience/Eurekah.com), 1–12.
11. Bump, N. J., Hackett, M., Hugunin, M., Seshagiri, S., Brady, K., Chen, P. (1995). Inhibition of ICE family proteases by baculovirus anti-apoptotic protein p35. Science 269, 1885–1888. doi: 10.1126/science.7569933
12. Cha-Um, S., Supaibulwattana, K., and Kirdmanee, C. (2009). Comparative effects of salt stress and extreme pH stress combined on glycinebetaine ccumulation, photosynthetic abilities and growth characters of two rice genotypes. Rice Sci. 16, 274–282. doi: 10.1016/s1672-6308(08)60091-60098
13. Chaves, M. M., Flexas, J., and Pinheiro, C. (2009). Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann. Bot. 103, 551–560. doi: 10.1093/aob/mcn125
14. Chawla, S., Jain, S., and Jain, V. (2013). Salinity induced oxidative stress and antioxidant system in salt-tolerant and salt-sensitive cultivars of rice (Oryza sativa L.). J. Plant Biochem. Biotechnol. 22, 27–34. doi: 10.1007/s13562-0120107-104
15. Cho, E., and Hong, C. (2006). Over-expression of tobacco NtHSP70-1 contributes to drought-stress tolerance in plants. Plant Cell Rep. 25, 349–358. doi: 10.1007/s00299-005-0093-92
16. Clem, R. J., Fechheimer, M., and Miller, L. K. (1991). Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254, 1388–1390. doi: 10.1126/science.1962198
17. Clem, R. J., and Miller, L. K. (1994). Control of programmed cell death by the baculovirus genes p35 and iap. Mol. Cell. Biol. 14, 5212–5222.
18. Cominelli, E., Conti, L., Tonelli, C., and Galbiati, M. (2013). Challenges and perspectives to improve crop drought and salinity tolerance. New Biotechnol. 30, 355–361. doi: 10.1016/j.nbt.2012.11.001
19. Considine, M. J., and Foyer, C. H. (2014). Antioxidants and Redox Signaling. Antioxid. Redox Signal. 21, 1305–1326. doi: 10.1089/ars.201 3.5665
20. Dickman, M. B., Park, Y. K., Oltersdorf, T., Li, W., Clemente, T., and French, R. (2001). Abrogation of disease development in plants expressing animal anti-apoptotic genes Proc.Natl.Acad.Sci.U.S.A.98, 6957–6962. doi: 10.1073/pnas.091108998
21. Dionisio-Sese, M. L., and Tobita, S. (1998). Antioxidant responses of rice seedlings to salinity stress. Plant Sci. 135, 1–9. doi: 10.1016/S0168-9452(98) 00025-9
22. Dionisio-Sese, M. L., and Tobita, S. (2000). Effects of salinity on sodium content and photosynthetic responses of rice seedlings differing in salt tolerance. J. Plant Physiol. 157, 54–58. doi: 10.1016/S0176-1617(00) 80135-2
23. Doukhanina, E. V., Chen, S., Van Der Zalm, E., Godzik, A., Reed, J., and Dickman, M. B. (2006). Identification and functional characterization of the BAG protein family in Arabidopsis thaliana. J. Biol. Chem. 281, 18793–18801. doi: 10.1074/jbc.M511794200
24. Eckardt, N. A. (2009). The Future of Science: food and Water for Life. Plant Cell 21, 368–372. doi: 10.1105/tpc.109.066209
25. El-Hendawy, S. E., Ruan, Y., Hu, Y., and Schmidhalter, U. (2009). A Comparison of screening criteria for salt tolerance in wheat under field and controlled environmental conditions. J. Agronomy Crop Sci. 195, 356–367. doi: 10.1111/j.1439037X.2009.00372.x
26. Ellerbrock, R., Höhn, A., and Gerke, H. H. (1999). Characterization of soil organic matter from a sandy soil in relation to management practice using FT-IR spectroscopy. Plant Soil 213, 55–61. doi: 10.1023/A:1004511714538
27. Eynard, A., Lal, R., and Wiebe, K. (2005). Crop response in salt-affected soils. J. Sustain. Agric. 27, 5–50. doi: 10.1300/J064v27n01-03
28. FAO. (2009). Declaration of the World Summit on Food Security. 16– 18 November, Rome. Available at: http://www.fao.org/wsfs/world-summit/wsfs-challenges/en/.
29. FAO. (2012). World Water Day 2012 Celebration. UN Conference Centre, Bangkok, 22 March 2012. Available at: http://www.fao.org/asiapacific/rap/home/meetings/list/detail/en/?meetings_id = 637&year = 2012.
30. Foyer, C. H., and Noctor, G. (2005). Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell Online 17, 1866–1875. doi: 10.1105/tpc.105.033589
31. Foyer, C. H., and Noctor, G. (2009). Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Redox Signal. 11, 861–905. doi: 10.1089/ars.2008.2177
32. Foyer, C. H., and Shigeoka, S. (2011). Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol. 155, 93–100. doi: 10.1104/pp.110.166181
33. Freitas, D., Coelho, M. F., Souza, M. Jr., Marques, A., and Ribeiro, E. B. (2007). Introduction of the anti-apoptotic baculovirus p35 gene in passion fruit induces herbicide tolerance, reduced bacterial lesions, but does not inhibits passion fruit woodiness disease progress induced by cowpea aphid-borne mosaic virus (CABMV). Biotechnol. Lett. 29, 79–87. doi: 10.1007/s10529-0069201-9209
34. Ghosh, N., Adak, M. K., Ghosh, P. D., Gupta, S., Sen Gupta, D. N., and Mandal, C. (2011). Differential responses of two rice varieties to salt stress. Plant Biotechnol. Rep. 5, 89–103. doi: 10.1007/s11816-010-0163-y
35. Gregorio, G. B., Senadhira, D., and Mendoza, R. D. (1997). Screening rice for salinity tolerance. IRRI Discussion Paper Series No. 22, 1–30.
36. Griffiths, P. R. (1975). Chemical Infrared Fourier Transform Spectroscopy. New York: Wiley-Interscience.
37. Hartl, F. U., Bracher, A., and Hayer-Hartl, M. (2011). Molecular chaperones in protein folding and proteostasis. Nature 475, 324–332. doi: 10.1038/nature10317
38. Heenan, D. P., Lewin, L. G., and Mccaffery, D. W. (1988). Salinity tolerance in rice varieties at different growth stages Aust. J. Exp. Agric. 28, 343–349. doi: 10.1071/EA9880343
39. Hoang, T. M. L. (2014). Engineering salinity tolerance in rice by manipulation of exogenous expression of cell death regulators. Ph.D. thesis, Queensland University of Technology, Queensland.
40. Hoang, T. M. L., Williams, B., Khanna, H., Dale, J., and Mundree, S. G. (2014). Physiological basis of salt stress tolerance in rice expressing the antiapoptotic gene SfIAP. Funct. Plant Biol. 41, 1168–1177. doi: 10.1071/FP 13308
41. Hossain, M., and Fischer, K. S. (1995). Rice research for food security and sustainable agricultural development in Asia: achievements and future challenges. GeoJ. 35, 286–298. doi: 10.1007/BF00989136
42. James, R. A., Munns, R., Von Caemmerer, S., Trejo, C., Miller, C., and Condon, T. (2006). Photosynthetic capacity is related to the cellular and subcellular partitioning of Na+, K+ and Cl-in salt-affected barley and durum wheat. Plant Cell Environ. 29, 2185–2197. doi: 10.1111/j.1365-3040.2006. 01592.x
43. Joly, A., Wettstein, G., Mignot, G., Ghiringhelli, F., and Garrido, C. (2010). Dual role of heat shock proteins as regulators of apoptosis and innate immunity. J. Innate Immun. 2, 238–247. doi: 10.1159/000296508
44. Kabbage, M., and Dickman, M. B. (2008). The BAGproteins: a ubiquitous family of chaperone regulators. Cell. Mol. Life Sci. 65, 1390–1402. doi: 10.1007/s00018008-7535-2
45. Khush, G. (2005). What it will take to Feed 5.0 Billion Rice consumers in 2030. Plant Mol. Biol. 59, 1–6. doi: 10.1007/s11103-005-2159-2155
46. Lafitte, R. (2002). Relationship between leaf relative water content during reproductive stage water deficit and grain formation in rice. Field Crops Res. 76, 165–74. doi: 10.1016/S0378-4290(02)00037-0
47. Lee, I. S., Kim, D. S., Lee, S. J., Song, H. S., Lim, Y. P., and Lee, Y. I. (2003). Selection and characterizations of radiation-induced salinitytolerant lines in rice. Breed. Sci. 53, 313–318. doi: 10.1270/jsbbs.53.313
48. Li, W., and Dickman, M. B. (2004). Abiotic stress induces apoptoticlike features in tobacco that is inhibited by expression of human Bcl-2. Biotechnol. Lett. 26, 87–95. doi: 10.1023/B:BILE.0000012896.7 6432.ba
49. Lincoln,J.E.,Craig,R.,Overduin,B.,Smith,K.,Bostock,R.,andGilchrist, D. G. (2002). Expression of the anti-apoptotic baculovirus p35 gene in tomato blocks programmed cell death and provides broad-spectrum resistance to disease. Proc. Natl. Acad. Sci. U.S.A. 99, 15217–15221. doi: 10.1073/pnas. 232579799
50. Long, S. P., Zhu, X.-G., Naidu, S. L., and Ort, D. R. (2006). Can improvement in photosynthesis increase crop yields? Plant Cell Environ. 29, 315–330. doi: 10.1111/j.1365-3040.2005.01493.x
51. + toxicity: the basis of cellular K+/Na+Ratios. Ann. Bot. 84, 123–133. doi: 10.1006/anbo.1999.0912
52. Meissl, K., Smidt, E., and Schwanninger, M. (2007). Prediction of humic acid content and respiration activity of biogenic waste by means of Fourier transform infrared (FTIR) spectra and partial least squares regression (PLS-R) models. Talanta 72, 791–799. doi: 10.1016/j.talanta.2006.12.005
53. Miller, G. A. D., Suzuki, N., Ciftci-Yilmaz, S., and Mittler, R. O. N. (2010). Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 33, 453–467. doi: 10.1111/j.1365-3040.2009. 02041.x
54. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405–410. doi: 10.1016/S1360-1385(02)02312-9
55. 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
56. Moradi, F., and Ismail, A. M. (2007). Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann. Bot. 99, 1161–1173. doi: 10.1093/aob/mcm052
57. Munns, R. (2011). “Plant adaptations to salt and water stress: differences and commonalities,” in Advances in Botanical Research, ed. T. Ismail (Waltham, MA: Academic Press), 1–32.
58. Munns, R., James, R. A., and Läuchli, A. (2006). Approaches to increasing the salt tolerance of wheat and other cereals. J. Exp. Bot. 57, 1025–1043. doi: 10.1093/jxb/erj100
59. Munns, R., and Tester, M. (2008). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651–681. doi: 10.1146/annurev.arplant.59.032607. 092911
60. Noctor, G., Mhamdi, A., and Foyer, C. H. (2014). The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiol. 164, 1636–1648. doi: 10.1104/pp.113.233478
61. Rhoads, D. M., Umbach, A. L., Subbaiah, C. C., and Siedow, J. N. (2006). Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol. 141, 357–366. doi: 10.1104/pp.106.079129
62. + ratios through the inhibition of Na+ uptake and transport to the shoots of Jatropha curcas plants. J. Plant Nutr. Soil Sci. 176, 157–164. doi: 10.1002/jpln.201200230
63. Sah, N. K., Taneja, T. K., Pathak, N., Begum, R., Athar, M., and Hasnain, S. E. (1999). The baculovirus anti-apoptotic p35 gene also functions via an oxidant-dependent pathway. Proc. Natl. Acad. Sci. U.S.A. 96, 4838–4843. doi: 10.1073/pnas.96. 9.4838
64. Sondermann, H., Scheufler, C., Schneider, C., Hohfeld, J., Hartl, F. U., and Moarefi, I. (2001). Structure of a Bag/Hsc70 complex: convergent functional evolution of Hsp70 nucleotide exchange factors. Science 291, 1553–1557. doi: 10.1126/science.1057268
65. Sussman, M. (1994). Molecular analysis of protein in the plant plasma membrane. Annu Rev. Plant Physiol. Plant Mol. Biol. 45, 211–234. doi: 10.1146/annurev.pp.45.060194.001235
66. Takayama, S., and Reed, J. C. (2001). Molecular chaperone targeting and regulation by BAG family proteins. Nat. Cell Biol. 3, E237–E241. doi: 10.1038/350 82637
67. UNFPA. (2014). Linking Population, Poverty and Development [Online]. Available: http://www.unfpa.org/pds/trends.htm [accessed February 8, 2014].
68. USDA. (2013). Bibliography on Salt Tolerance. Fibres, Grains and Special Crops. Riverside, CA: George E.Brown, Jr. Salinity Lab. US Department Agriculture, Agriculture Research Service.
69. Wang, Z., Song, J., Zhang, Y., Yang, B., and Chen, S. (2009). Expression of baculovirus anti-apoptotic p35 gene in tobacco enhances tolerance to abiotic stress. Biotechnol. Lett. 31, 585–589. doi: 10.1007/s10529-008-9879-y
70. Williams, B., and Dickman, M. (2008). Plant programmed cell death: can’t live with it; can’t live without it. Mol. Plant Pathol. 9, 531–544. doi: 10.1111/j.13643703.2008.00473.x
71. Williams, B., Kabbage, M., Britt, R., and Dickman, M. B. (2010). AtBAG7, an Arabidopsis Bcl-2–associated athanogene, resides in the endoplasmic reticulum and is involved in the unfolded protein response. Proc. Natl. Acad. Sci. U.S.A. 107, 6088–6093. doi: 10.1073/pnas.0912670107
72. Williams, B., Verchot, J., and Dickman, M. (2014). When supply does not meet demand-ER stress and plant programmed cell death. Front. Plant Sci. 5:211. doi: 10.3389/fpls.2014.00211
73. Xue, D., and Horvitz, H. R. (1995). Inhibition of the Caenorhabditis elegans celldeath protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature 377, 248–251. doi: 10.1038/377248a0
74. Yang, J., and Yen, H. E. (2002). Early salt stress effects on the changes in chemical composition in leaves of ice plant and Arabidopsis. A Fourier transform infrared spectroscopy study. Plant Physiol. 130, 1032–1042. doi: 10.1104/pp.004325
75. Zeng, L., Shannon, M. C., and Grieve, C. M. (2002). Evaluation of salt tolerance in rice genotypes by multiple agronomic parameters. Euphytica 127, 235–245. doi: 10.1023/A:1020262932277
76. Zeng, L., Shannon, M. C., and Lesch, S. M. (2001). Timing of salinity stress affects rice growth and yield components. Agric. Water Manag. 48, 191–206. doi: 10.1016/S0378-3774(00)00146-3
77. Zeng, L. H., Poss, J. A., Wilson, C., Draz, A. S. E., Gregorio, G. B., and Grieve, C. M. (2003). Evaluation of salt tolerance in rice genotypes by physiological characters. Euphytica 129, 281–292. doi: 10.1023/A:1022248522536
78. Zhu, J.-K. (2001). Plant salt tolerance. Trends Plant Sci. 6, 66–71. doi: 10.1016/S1360-1385(00)01838-0
79. Zhu, J., Fu, X., Koo, Y. D., Zhu, J. K., Jenney, F. E. J., Adams, M. W., et al. (2007). An enhancer mutant of Arabidopsis salt overly sensitive 3 mediates both ion homeostasis and the oxidative stress response. MolCellBiol.27, 5214–5224. doi: 10.1128/MCB.01989-06