UV-C-irradiated Arabidopsis and tobacco emit volatiles that trigger genomic instability in neighboring plants

Plant Cell

Volumn 23, Issue 10, 2011, Pages 3842-3852

  Yao, Youli ^a   Danna, Cristian H ^b,c   Zemp, Franz J ^d   Titov, Viktor ^a   Ciftci, Ozan Nazim ^a   Przybylski, Roman ^a   Ausubel, Frederick M ^b,c   Kovalchuk, Igor ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 82755195640     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.089003     Document Type: Article

References (53)

1. Agrawal, G.K., Jwa, N.S., Shibato, J., Han, O., Iwahashi, H., and Rakwal, R. (2003). Diverse environmental cues transiently regulate OsOPR1 of the "octadecanoid pathway" revealing its importance in rice defense/stress and development. Biochem. Biophys. Res. Commun. 310: 1073-1082.
2. Alonso, J.M., Hirayama, T., Roman, G., Nourizadeh, S., and Ecker, J.R. (1999). EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284: 2148-2152.
3. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
4. Apostol, I., Heinstein, P.F., and Low, P.S. (1989). Rapid stimulation of an oxidative burst during elicitation of cultured plant cells: Role in defense and signal transduction. Plant Physiol. 90: 109-116.
5. Attaran, E., Zeier, T.E., Griebel, T., and Zeier, J. (2009). Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21: 954-971.
6. Baldwin, I.T., Halitschke, R., Paschold, A., von Dahl, C.C., and Preston, C.A. (2006). Volatile signaling in plant-plant interactions: "Talking trees" in the genomics era. Science 311: 812-815.
7. Bowling, S.A., Clarke, J.D., Liu, Y., Klessig, D.F., and Dong, X. (1997). The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9: 1573-1584.
8. Bowling, S.A., Guo, A., Cao, H., Gordon, A.S., Klessig, D.F., and Dong, X. (1994). A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell 6: 1845-1857.
9. Boyko, A., Blevins, T., Yao, Y., Golubov, A., Bilichak, A., Ilnytskyy, Y., Hollunder, J., Meins, F., Jr., and Kovalchuk, I. (2010a). Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins. PLoS ONE 5: e9514.
10. Boyko, A., Golubov, A., Bilichak, A., and Kovalchuk, I. (2010b). Chlorine ions but not sodium ions alter genome stability of Arabidopsis thaliana. Plant Cell Physiol. 51: 1066-1078.
11. Boyko, A., Greer, M., and Kovalchuk, I. (2006a). Acute exposure to UVB has a more profound effect on plant genome stability than chronic exposure. Mutat. Res. 602: 100-109.
12. Boyko, A., Hudson, D., Bhomkar, P., Kathiria, P., and Kovalchuk, I. (2006b). Increase of homologous recombination frequency in vascular tissue of Arabidopsis plants exposed to salt stress. Plant Cell Physiol. 47: 736-742.
13. Boyko, A., Kathiria, P., Zemp, F.J., Yao, Y., Pogribny, I., and Kovalchuk, I. (2007). Transgenerational changes in the genome stability and methylation in pathogen-infected plants: (virus-induced plant genome instability). Nucleic Acids Res. 35: 1714-1725.
14. Boyko, A., and Kovalchuk, I. (2010). Transgenerational response to stress in Arabidopsis thaliana. Plant Signal. Behav. 5: 995-998.
15. Boyko, A., Zemp, F., Filkowski, J., and Kovalchuk, I. (2006c). Double-strand break repair in plants is developmentally regulated. Plant Physiol. 141: 488-497.
16. Cao, H., Glazebrook, J., Clarke, J.D., Volko, S., and Dong, X. (1997). The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57-63.
17. Caputo, C., Rutitzky, M., and Ballaré, C.L. (2006). Solar ultraviolet-B radiation alters the attractiveness of Arabidopsis plants to diamondback moths (Plutella xylostella L.): Impacts on oviposition and involvement of the jasmonic acid pathway. Oecologia 149: 81-90.
18. Clarke, J.D., Liu, Y., Klessig, D.F., and Dong, X. (1998). Uncoupling PR gene expression from NPR1 and bacterial resistance: Characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell 10: 557-569.
19. Clarke, J.D., Volko, S.M., Ledford, H., Ausubel, F.M., and Dong, X. (2000). Roles of salicylic acid, jasmonic acid, and ethylene in cprinduced resistance in Arabidopsis. Plant Cell 12: 2175-2190.
20. Clarke, S.M., Cristescu, S.M., Miersch, O., Harren, F.J., Wasternack, C., and Mur, L.A. (2009). Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol. 182: 175-187.
21. Danon, A., Rotari, V.I., Gordon, A., Mailhac, N., and Gallois, P. (2004). 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. 279: 779-787.
22. Demkura, P.V., Abdala, G., Baldwin, I.T., and Ballaré, C.L. (2010). Jasmonate-dependent and -independent pathways mediate specific effects of solar ultraviolet B radiation on leaf phenolics and antiherbivore defense. Plant Physiol. 152: 1084-1095.
23. Durrant, W.E., Wang, S., and Dong, X. (2007). Arabidopsis SNI1 and RAD51D regulate both gene transcription and DNA recombination during the defense response. Proc. Natl. Acad. Sci. USA 104: 4223-4227.
24. Farmer, E.E., and Ryan, C.A. (1990). Interplant communication: Airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc. Natl. Acad. Sci. USA 87: 7713-7716.
25. Filkowski, J., Kovalchuk, O., and Kovalchuk, I. (2004). Genome stability of vtc1, tt4, and tt5 Arabidopsis thaliana mutants impaired in protection against oxidative stress. Plant J. 38: 60-69.
26. Foggo, A., Higgins, S., Wargent, J.J., and Coleman, R.A. (2007). Tritrophic consequences of UV-B exposure: Plants, herbivores and parasitoids. Oecologia 154: 505-512.
27. Grant, M., and Lamb, C. (2006). Systemic immunity. Curr. Opin. Plant Biol. 9: 414-420.
28. Green, R., and Fluhr, R. (1995). UV-B-induced PR-1 accumulation is mediated by active oxygen species. Plant Cell 7: 203-212.
29. Heil, M., and Silva Bueno, J.C. (2007). Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. USA 104: 5467-5472.
30. Ilnytskyy, Y., Boyko, A., and Kovalchuk, I. (2004). Luciferasebased transgenic recombination assay is more sensitive than betaglucoronidase- based. Mutat. Res. 559: 189-197.
31. Jenkins, G.I. (2009). Signal transduction in responses to UV-B radiation. Annu. Rev. Plant Biol. 60: 407-431.
32. Jung, H.W., Tschaplinski, T.J., Wang, L., Glazebrook, J., and Greenberg, J.T. (2009). Priming in systemic plant immunity. Science 324: 89-91.
33. Kathiria, P., and Kovalchuk, I. (2010). Reporter gene-based recombination lines for studies of genome stability. Methods Mol. Biol. 631: 243-252.
34. Kathiria, P., Sidler, C., Golubov, A., Kalischuk, M., Kawchuk, L.M., and Kovalchuk, I. (2010). Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial, and fungal pathogens in the progeny of infected tobacco plants. Plant Physiol. 153: 1859-1870.
35. Kirik, V., Bouyer, D., Schöbinger, U., Bechtold, N., Herzog, M., Bonneville, J.M., and Hülskamp, M. (2001). CPR5 is involved in cell proliferation and cell death control and encodes a novel transmembrane protein. Curr. Biol. 11: 1891-1895.
36. Kovalchuk, I., Kovalchuk, O., Kalck, V., Boyko, V., Filkowski, J., Heinlein, M., and Hohn, B. (2003). Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423: 760-762.
37. Love, A.J., Yun, B.W., Laval, V., Loake, G.J., and Milner, J.J. (2005). Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol. 139: 935-948.
38. Martínez, C., Pons, E., Prats, G., and León, J. (2004). Salicylic acid regulates flowering time and links defence responses and reproductive development. Plant J. 37: 209-217.
39. Park, S.W., Kaimoyo, E., Kumar, D., Mosher, S., and Klessig, D.F. (2007). Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318: 113-116.
40. Park, S.W., Liu, P.P., Forouhar, F., Vlot, A.C., Tong, L., Tietjen, K., and Klessig, D.F. (2009). Use of a synthetic salicylic acid analog to investigate the roles of methyl salicylate and its esterases in plant disease resistance. J. Biol. Chem. 284: 7307-7317.
41. Puchta, H. (2005). The repair of double-strand breaks in plants: Mechanisms and consequences for genome evolution. J. Exp. Bot. 56: 1-14.
42. Rao, M.V., Lee, H., Creelman, R.A., Mullet, J.E., and Davis, K.R. (2000). Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12: 1633-1646.
43. Ries, G., Heller, W., Puchta, H., Sandermann, H., Seidlitz, H.K., and Hohn, B. (2000). Elevated UV-B radiation reduces genome stability in plants. Nature 406: 98-101.
44. Rochette, P.J., Lacoste, S., Therrien, J.P., Bastien, N., Brash, D.E., and Drouin, R. (2009). Influence of cytosine methylation on ultravioletinduced cyclobutane pyrimidine dimer formation in genomic DNA. Mutat. Res. 665: 7-13.
45. Ryan, C.A., and Moura, D.S. (2002). Systemic wound signaling in plants: A new perception. Proc. Natl. Acad. Sci. USA 99: 6519-6520.
46. Santner, A., Calderon-Villalobos, L.I., and Estelle, M. (2009). Plant hormones are versatile chemical regulators of plant growth. Nat. Chem. Biol. 5: 301-307.
47. Shulaev, V., Leon, J., and Raskin, I. (1995). Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? Plant Cell 7: 1691-1701.
48. Staswick, P.E., Tiryaki, I., and Rowe, M.L. (2002). Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14: 1405-1415.
49. Stratmann, J.W., Stelmach, B.A., Weiler, E.W., and Ryan, C.A. (2000). UVB/UVA radiation activates a 48 kDa myelin basic protein kinase and potentiates wound signaling in tomato leaves. Photochem. Photobiol. 71: 116-123.
50. Wang, S., Durrant, W.E., Song, J., Spivey, N.W., and Dong, X. (2010). Arabidopsis BRCA2 and RAD51 proteins are specifically involved in defense gene transcription during plant immune responses. Proc. Natl. Acad. Sci. USA 107: 22716-22721.
51. Weber, W., Daoud-El Baba, M., and Fussenegger, M. (2007). Synthetic ecosystems based on airborne inter- and intrakingdom communication. Proc. Natl. Acad. Sci. USA 104: 10435-10440.
52. Wildermuth, M.C., Dewdney, J., Wu, G., and Ausubel, F.M. (2001). Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562-565.
53. Yalpani, N., Leon, J., Lawton, M.A., and Raskin, I. (1993). Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiol. 103: 315-321.