The role of ROS signaling in cross-tolerance: From model to crop

Frontiers in Plant Science

Volumn 5, Issue DEC, 2014, Pages 1-6

  Perez, Llse Barrios ^a   Brown, Patrick J ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Acclimation; GST; Oxidative stress; Oxylipin; Quantitative disease resistance; Systemic resistance

Indexed keywords

EID: 84922014948     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00754     Document Type: Review

References (67)

1. Alam, M. M., Hasanuzzaman, M., Nahar, K., and Fujita, M. (2013). Exogenous salicylic acid ameliorates short-term drought stress in mustard (Brassica juncea L.) seedlings byup-regulating the antioxidant defense and glyoxalase system. Aust. J. Crop Sci. 7,1053-1063.
2. Apel, K., and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress, an,d signal transduction. Annu. Rev. Plant Biol. 55, 373-399. doi: 10.1146/annurev.arplant.55.031903.141701
3. Arasimowicz-Jelonek, M., Floryszak-Wieczorek, J., Drzewiecka, K., Chmielowska- Bak, J., Abramowski, D., and Izbianska, K. (2013). Aluminum induces cross-resistance of potato to Phytophthora infestans. Planta 239, 679-694. doi: 10.1007/s00425-013-2008-8
4. Baxter, A., Mittler, R., and Suzuki, N. (2014). ROS as key players in plant stress signalling. J. Exp. Bot. 65, 1229-1240. doi: 10.1093/jxb/ert375
5. Bechtold, U., Albihlal, W. S., Lawson, T., Fryer, M. J., Sparrow, P. A. C., Richard, etal. (2013). Arabidopsis HEAT SHOCK TRANSCRIPTION FACTORA1b overexpression enhances water productivity, resistance to drought, and infection. J. Exp. Bot. 64, 3467-3481. doi: 10.1093/jxb/ert185
6. Brosche, M., Blomster, T., Salojarvi, J., Cui, F., Sipari, N., Leppala, J., etal. (2014). Transcriptomics and functional genomics of ROS-induced cell death regulation by RADICAL-INDUCED CELL DEATH1. PLoS Genet. 10:e1004112. doi: 10.1371/journal.pgen.1004112
7. Brosche, M., Merilo, E., Mayer, F., Pechter, P., Puzorjova, I., Brader, G., et al.. Natural variation in ozone sensitivity among Arabidopsis thaliana accessions and its relation to stomatal conductance. Plant Cell Environ. 33, 914-925. doi: 10.1111/j.1365-3040.2010.02116.x
8. Brun, H., Chevre, A.-M., Fitt, B. D., Powers, S., Besnard, A.-L., Ermel, M., et al.. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol. 185, 285-299. doi: 10.1111/j.1469-8137.2009.03049.x
9. Buschmann, H., Fan, Z., and Sauerborn, J. (2005). Effect of resistance-inducing agents on sunflower (Helianthus annuus L.) and its infestation with the parasitic weed Orobanche cumana Wallr. J. PlantDis. Prot. 112, 386-397.
10. Ciftci-Yilmaz, S., Morsy, M. R., Song, L., Coutu, A., Krizek, B. A., Lewis, M. W., et al.. The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J. Biol. Chem. 282, 9260-9268. doi: 10.1074/jbc.M611093200
11. Constantino, N. N., Mastouri, F., Damarwinasis, R., Borrego, E. J., Moran-Diez, M. E., Kenerley, C. M., etal. (2013). Root-expressed maize lipoxygenase 3 negatively regulates induced systemic resistance to Colletotrichum graminicola in shoots. Front. PlantSci. 4:510. doi: 10.3389/fpls.2013.00510
12. Dann, E. K., Diers, B.W., and Hammerschmidt, R. (1999). Suppression of Sclerotinia stem rot of soybean bylactofen herbicide treatment. Phytopathology 89, 598-602. doi: 10.1094/PHYTO.1999.89.7.598
13. Davletova, S., Schlauch, K., Coutu, J., and Mittler, R. (2005). The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol. 139, 847-856. doi: 10.1104/pp.105.068254
14. Dean, J. D., Goodwin, P. H., and Hsiang, T. (2005). Induction of glutathione S- transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. J. Exp. Bot. 56, 1525-1533. doi: 10.1093/jxb/eri145
15. De Pinto, M. C., Locato, V., and De Gara, L. (2012). Redox regulation in plant programmed cell death. Plant Cell Environ. 35, 234-244. doi: 10.1111/j.1365-3040.2011.02387.x
16. Gadjev, I. (2006). Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141, 436-445. doi: 10.1104/pp.106.078717
17. Geetha, H. M., and Shetty, H. S. (2002). Induction of resistance in pearl millet against downy mildew disease caused bySclerospora graminicola using benzothiadiazole, calcium chloride and hydrogen peroxide—a comparative evaluation. Crop Prot. 601-610. doi: 10.1016/S0261-2194(01)00150-8
18. Gozzo, F., and Faoro, F. (2013). Systemic acquired resistance (50 years after discovery): moving from the lab to the field. J. Agric. Food Chem. 61,12473-12491. doi: 10.1021/jf404156x
19. Graham, M. Y. (2005). The diphenylether herbicide lactofen induces cell death and expression of defense-related genes in soybean. Plant Physiol. 139, 1784-1794. doi: 10.1104/pp.105.068676
20. Halliwell, B. (2006). Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol. 141, 312-322. doi: 10.1104/pp.106.0 77073
21. Hasanuzzaman, M., Alam, M. M., Nahar, K., Ahamed, K. U., and Fujita, M. (2014). Exogenous salicylic acid alleviates salt stress-induced oxidative damage in Brassica napus by enhancing the antioxidant defense and glyoxalase systems. Aust. J. Crop Sci. 8,631-639.
22. Hassan, I. A. (2006). Physiological and biochemical response of potato (Solanum tuberosum L. cv. Kara) to O3 and antioxidant chemicals: possible roles of antioxidant enzymes. Ann. Appl. Biol. 148, 197-206. doi: 10.1111/j.1744-7348.2006.00058.x
23. Hayat, Q., Hayat, S., Irfan, M., and Ahmad, A. (2010). Effect of exogenous salicylic acid under changing environment: a review. Environ. Exp. Bot. 68, 14-25. doi: 10.1016/j.envexpbot.2009.08.005
24. He, L., and Gao, Z. (2009). Pretreatment of seed with H2O2 enhances drought tolerance of wheat (Triticum aestivum L.) seedlings. Afr. J. Biotechnol. 8:22.
25. Herman, M. A. B., Davidson, J. K., and Smart, C. D. (2008). Induction of plant defense gene expression by plant activators and Pseudomonas syringae pv. tomato in greenhouse-grown tomatoes. Phytopathology 98, 1226-1232. doi: 10.1094/PHYTO-98-11-1226
26. Herms, S., Seehaus, K., Koehle, H., and Conrath, U. (2002). A strobilurin fungicide enhances the resistance of tobacco against tobacco mosaic virus and Pseudomonas syringae pv tabaci. Plant Physiol. 130, 120-127. doi: 10.1104/pp. 004432
27. Hyung, D., Lee, C., Kim, J.-H., Yoo, D., Seo, Y.-S., Jeong, S.-C., etal. (2014). Cross-family translational genomics of abiotic stress-responsive genes between Arabidopsis and Medicago truncatula. PLoS ONE 9:e91721. doi: 10.1371/jour-nal.pone.0091721
28. Iriti, M., Rabotti, G., De Ascensao, A., and Faoro, F. (2003). Benzothiadiazole- induced resistance modulates ozone tolerance.J. Agric. Food Chem. 51, 43084314. doi: 10.1021/jf034308w
29. Iseki, K., Homma, K., Endo, T., and Shiraiwa, T. (2013). Genotypic diversity of cross-tolerance to oxidative and drought stresses in rice seedlings evaluated by the maximum quantum yield of photosystem II and membrane stability. Plant Prod. Sci. 16, 295-304. doi: 10.1626/pps.16.295
30. Iseki, K., Homma, K., Shiraiwa, T., Jongdee, B., and Mekwatanakarn, P. (2014). The effects of cross-tolerance to oxidative stress and drought stress on rice dry matter production under aerobic conditions. Field Crops Res. 163, 18-23. doi: 10.1016/j.fcr.2014.04.012
31. Kobayashi, M., Ohura, I., Kawakita, K., Yokota, N., Fujiwara, M., Shimamoto, K., etal. (2007). Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19, 1065-1080. doi: 10.1105/tpc.106.048884
32. Kong, J., Dong, Y., Xu, L., Liu, S., and Bai, X. (2014). Effects of foliar application of salicylic acid and nitric oxide in alleviating iron deficiency induced chlorosis of Arachis hypogaea L. Bot. Stud. 55, 9-10. doi: 10.1186/1999-3110-55-9
33. Kump, K. L., Bradbury, P. J., Wisser, R. J., Buckler, E. S., Belcher, A. R., Oropeza- Rosas, M. A., etal. (2011). Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat. Genet. 43, 163-168. doi: 10.1038/ng.747
34. Li, J., Brader, G., and Palva, E. T. (2004). The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell Online 16, 319-331. doi: 10.1105/tpc.016980
35. Liu, F., Xu, W., Wei, Q., Zhang, Z., Xing, Z., Tan, L., et al. (2010). Gene expression profiles deciphering rice phenotypic variation between Nipponbare (Japonica) and 93-11 (Indica) during oxidative stress. PLoS ONE 5:e8632. doi: 10.1371/journal.pone.0008632
36. Malan, C., Greyling, M., and Gressel, J. (1990). Correlation between CuZn superoxide dismutase and glutathione reductase, and environmental and xenobiotic stress tolerance in maize inbreds. Plant Sci. 69, 157-166. doi: 10.1016/0168-9452(90)90114-4
37. Miller, G., and Mittler, R. (2006). Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann. Bot. 98, 279-288. doi: 10.1093/aob/mcl107
38. Mittal, D., Madhyastha, D. A., and Grover, A. (2012). Genome-wide transcriptional profiles during temperature and oxidative stress reveal coordinated expression patterns and overlapping regulons in rice. PLoS ONE 7:e40899. doi: 10.1371/journal.pone.0040899
39. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7,405-410.doi:10.1016/S1360-1385(02)02312-9
40. Mittler, R. (2006). Abiotic stress, the field environment and stress combination. Trends Plant Sci. 11, 15-19. doi: 10.1016/j.tplants.2005.11.002
41. Mittler, R., Kim, Y., Song, L., Coutu, J., Coutu, A., Ciftci-Yilmaz, S., et al. (2006). Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett. 580, 6537-6542. doi: 10.1016/j.febslet.2006.11.002
42. Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V. B., Vandepoele, K., et al. (2011). ROS signaling: the new wave? Trends Plant Sci. 16, 300-309. doi: 10.1016/j.tplants.2011.03.007
43. Ort, D. R., Ainsworth, E. A., Aldea, M., Allen, D. J., Bernacchi, C. J., Berenbaum, M. R., et al. (2006).“SoyFACE: the Effects andInteractions ofElevated [CO2] and [O3] on Soybean,” in Managed Ecosystems and CO2 Ecological Studies, eds P. D. J. Nosberger, P. D. S. P. Long, P. D. R. J. Norby, P. D. M. Stitt, P. D. G. R. Hendrey, and D. H. Blum (Heidelberg: Springer), 71-86.
44. Pandey, S. P., and Somssich, I. E. (2009). The role of WRKY transcription factors in plant immunity. PlantPhysiol. 150, 1648-1655. doi: 10.1104/pp.109.138990
45. Poland, J. A., Balint-Kurti, P. J., Wisser, R. J., Pratt, R. C., and Nelson, R. J. (2009). Shades of gray: the world of quantitative disease resistance. Trends Plant Sci. 14, 21-29. doi: 10.1016/j.tplants.2008.10.006
46. Puckette, M. C., Weng, H., and Mahalingam, R. (2007). Physiological and biochemical responses to acute ozone-induced oxidative stress in Medicago truncatula. PlantPhysiol. Biochem. 45, 70-79. doi: 10.1016/j.plaphy.2006.12.004
47. Rao, M.V., and Davis, K.R. (1999). Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J. 17, 603-614. doi: 10.1046/j.1365-313X.1999.00400.x
48. Riechers, D. E., Kreuz, K., and Zhang, Q. (2010). Detoxification without intoxication: herbicide safeners activate plant defense gene expression. PlantPhysiol. 153, 3-13. doi: 10.1104/pp.110.153601
49. Rizhsky, L. (2004). The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J. Biol. Chem. 279, 11736-11743. doi: 10.1074/jbc.M313350200
50. Sakamoto, H., Maruyama, K., Sakuma, Y., Meshi, T., Iwabuchi, M., Shinozaki, K., et al. (2004). Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol. 136,2734-2746. doi: 10.1104/pp.104.046599
51. Sandermann, H. Jr. (1996). Ozone and plant health. Annu. Rev. Phytopathol. 34, 347-366. doi: 10.1146/annurev.phyto.34.1.347
52. Scarpeci, T., Zanor, M., Bernd Mueller, R., and Valle, E. (2013). Overexpression of AtWRKY30 enhances abiotic stress tolerance during early growth stages in Arabidopsis thaliana. Plant Mol. Biol. 83, 265-277. doi: 10.1007/s11103-013-0090-8
53. Shaaltiel, Y., Glazer, A., Bocion, P. F., and Gressel, J. (1988). Cross tolerance to herbicidal and environmental oxidants of plant biotypes tolerant to paraquat, sulfur dioxide, and ozone. Pestic. Biochem. Physiol. 31, 13-23. doi: 10.1016/0048-3575(88)90024-7.
54. Shabala, S., Baekgaard, L., Shabala, L., Fuglsang, A., Babourina, O., Palmgren, M., et al. (2011). Plasma membrane Ca2+ transporters mediate virus-induced acquired resistance to oxidative stress. Plant Cell Environ. 34, 406-417. doi: 10.1111/j.1365-3040.2010.02251.x
55. Shaik, R., and Ramakrishna, W. (2013). Genes and co-expression modules common to drought and bacterial stress responses in Arabidopsis and rice. PLoS ONE 8:e77261. doi: 10.1371/journal.pone.0077261
56. Shi, H., Wang, X., Ye, T., Cheng, F., Deng, J., Yang, P., et al. (2014). The Cysteine2/Histidine2-type transcription factor ZINCFINGER OFARABIDOPSIS THALIANA6 modulates biotic and abiotic stress responses by activating salicylic acid-related genes and C-REPEAT-BINDING FACTOR genes in Arabidopsis. Plant Physiol. 165,1367-1379. doi: 10.1104/pp.114.242404
57. Siddiqui, M. H., Al-Whaibi, M. H., Ali, H. M., Sakran, A. M., Basalah, M. O., and AlKhaishany, M. Y. Y. (2013). Mitigation of nickel stress by the exogenous application of salicylic acid and nitric oxide in wheat. Aust. J. Crop Sci. 7, 17801788.
58. Singh, A., Srivastava, A. K., and Singh, A. K. (2013). Exogenous application of salicylic acid to alleviate the toxic effects of insecticides in Vicia faba L. Environ. Toxicol. 28, 666-672. doi: 10.1002/tox.20745
59. Sudhakar, N., Nagendra-Prasad, D., Mohan, N., and Murugesan, K. (2007). Induction of systemic resistance in Lycopersicon esculentum cv. PKM1 (tomato) against cucumber mosaic virus by using ozone. J. Virol. Methods 139, 71-77. doi: 10.1016/j.jviromet.2006.09.013
60. Tippmann, H. F., Schluter, U., Collinge, D. B., and Teixeira da Silva, J. A. (2006). Common themes in biotic and abiotic stress signalling in plants. Floric. Ornam. PlantBiotechnol. 3, 52-67.
61. Vainonen, J. P., and Kangasjarvi, J. (2014). Plant signaling in acute ozone exposure. Plant Cell Environ. doi: 10.1111/pce.12273[Epub ahead of print].
62. Wagner, U., Edwards, R., Dixon, D. P., and Mauch, F. (2002). Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol. Biol. 49, 515-532. doi: 10.1023/A:1015557300450
63. Wahid, A., Perveen, M., Gelani, S., and Basra, S. M. (2007). Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. J. Plant Physiol. 164, 283-294. doi: 10.1016/j.jplph.2006.01.005
64. Wisser, R. J., Kolkman, J. M., Patzoldt, M. E., Holland, J. B., Yu, J., Krakowsky, M., et al. (2011). Multivariate analysis of maize disease resistances suggests a pleiotropic genetic basis and implicates a GST gene. Proc. Natl. Acad. Sci. U.S.A. 108, 7339-7344. doi: 10.1073/pnas.1011739108
65. Wisser, R. J., Sun, Q., Hulbert, S. H., Kresovich, S., and Nelson, R. J. (2005). Identification and characterization of regions of the rice genome associated With broad-spectrum, quantitative disease resistance. Genetics 169, 2277-2293. doi: 10.1534/genetics.104.036327
66. Wohlgemuth, H., Mittelstrass, K., Kschieschan, S., Bender, J., Weigel, H.-J., Overmyer, K., et al. (2002). Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. PlantCell Environ. 25, 717-726. doi: 10.1046/j.1365-3040.2002.00859.x
67. Yalpani, N., Enyedi, A. J., Leon, J., and Raskin, I. (1994). Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco. Planta 193, 372-376. doi: 10.1007/BF00201815