Overcoming Glucosinolate-Myrosinase-Isothiocyanate Defense System by Plant Pathogenic Fungi

Öz

Natural compounds play an important role in shaping living plant responses. The resistance of plants is dependent on the formation and production of antimicrobial compounds of secondary metabolites. Glucosinolates (GSLs) are the main source of phytoanticipin in Brassicaceae and other plant families. The biological activity of glucosinolates are dependent on the release of various toxic compounds due to hydrolysis by myrosinase, isothiocyanate (ITC) is glucosinolate-breakdown products that inhibit the growth of microorganisms. In this review, we aim to understand how fungal pathogens overcome the glucosinolate-myrosinase-isothiocyanate system. The pathogens overwhelm the plant's defense system in various ways and disable each component of the system. Many plant pathogens may not cause tissue damage or activation of the glucosinolate-myrosinase-isothiocyanate system, others degrade or transforms the intact GSLs to less or non-toxic products, or inhibit the hydrolysis of GSLs catalyzed by myrosinase, or formed special mechanisms to detoxify toxic GSLs degradation products.

Anahtar Kelimeler

• Secondary metabolite
• Glucosinolate
• Myrosinase
• Isothiocyanate

References

1. Turner, J.G., Ellis, C., Devoto A. (2002). The jasmonate signal pathway. Am Soc Plant Biolthe Plant Cell. 14(1). doi:https://doi.org/10.1105/tpc.000679
2. Bednarek, P., Bednarek, M., Svatos, A., Schneider, B., Doubsky, J., Mansurova, M., Humphry, M., Consonni, Ch., Panstruga, R., Sanchez-Vallet, A., Molina, A., Schulze-Lefert, P. (2009). A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science, 323(5910),101 106. doi:https://doi.org/10.1126/science.1163732
3. Pastor, V., Luna E., Mauch-Mani, B., Ton, J., Flores, V. (2013). Primed plants to do not forget. Environ Exp. Bot., 94, 46-56. doi:https://doi.org/10.1016/j.envexpbot.2012.02.013
4. Kliebenstein, D.J. (2004). Secondary metabolites and plant/environment interactions: a view through Arabidopsis thaliana tinged glasses. Plant, Cell and Environment, 27(6), 675-684. doi:https://doi.org/10.1111/j.1365-3040.2004.01180.x
5. Stotz, H.U., Sawada, Y., Shimada, Y. (2011). Role of camalexin, indole glucosinolate-derived isothiocyanates in defense of Arabidopsis against Sclerotinia sclerotiorum. Plant Journal, 67(1), 81-93. doi:https://doi.org/10.1111/j.1365-313X.2011.04578.x
6. Kovalchuk, A., Kerio, S., Oghenekaro, A.O., Jaber, E., Raffaello, T., Asiegbu, F.O. (2013). Antimicrobial defenses and resistance in forest trees: challenges and perspectives in a genomic era. Annu Rev Phytopathol, 51, 221-244. doi:https://doi.org/10.1146/annurev-phyto-082712-102307
7. Van Etten, H.D., Mansfield, J.W., Bailey, J.A., Farmer, E.E. (1994). Two classes of plant antibiotics: phytoalexins versus phytoanticipins. Plant Cell, 6(9), 1191 1192. doi:https://dx.doi.org/10.1105%2Ftpc.6.9.1191
8. Merillon, J.M., Ramawat, K.G. (2017). Advances in botanical research: Glucosinolates. Springer International Publishing, Switzerland, pp. 473.

9. Rodman, J.E., Karol, K.G., Price, R.A. Systema, K.J. (1996). Molecules morphology, and Dahlgren's expanded order Capparales, Systematic Botany, 21(3), 289-307. doi:https://doi.org/10.2307/2419660
10. Fahey, J.W., Zalcmann, A.T., Talalay, P. (2001). The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry, 56(1), 5-51. doi:https://doi.org/10.1016/S0031-9422(00)00316-2
11. Hopkins, R.J., Van Dam, N.M., Van Loon, J.A. (2009). Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annual Review of Phytopathology, 54, 57-83. doi:https://doi.org/10.1146/annurev.ento.54.110807.090623
12. Agerbırk, N., Olsen, S. (1998). Initial, and final products, nitriles, and ascorbates produced in myrosinase-catalyzed hydrolysis of indole glucosinolates. J Agric Food Chem, 46(4), 1563–1571. doi:https://doi.org/10.1021/jf9708498
13. Grubb, D., Abel, S. (2006). Glucosinolate metabolism and its control. Trends in Plant Science, 11(2), 89-100. doi:https://doi.org/10.1016/j.tplants.2005.12.006
14. Bones, A.M., Rossiter, J.T. (1996). The myrosinase-glucosinolate system its organization and biochemistry. Physiologia Plantarum, 97(1), 194-208. doi:https://doi.org/10.1111/j.1399-3054.1996.tb00497.x
15. Brown, P.D., Morra, M.J., (1996). Hydrolysis products of glucosinolates in Brassica napus tissues as inhibitors of seed germination. Plant and Soil, 181(2), 307-316. doi:https://doi.org/10.1007/BF00012065
16. Wittstock, U., Halkier, B.A. (2002). Glucosinolate research in the Arabidopsis era. Trends in Plant Science., 7(6), 263-270. doi:https://doi.org/10.1016/S1360-1385(02)02273-2
17. Halkier, B.A., Gerchenzon, J. (2006). Biology and biochemistry of glucosinolates. Annu Rev Plant Biol., 57, 303-333. doi:https://doi.org/10.1146/annurev.arplant.57.032905.105228
18. Redovnikovic, I.R., Glivetic, T., Vorkapic-Furac, J. (2008). Glucosinolates and their potential role in the ant. Periodicumbiologorum., 110(4), 297-309.
19. Kliebenstein, D.J., Kroymann, J., Thomas, M.O. (2005). The glucosinolate-myrosinase system in an ecological and evolutionary context. Curr Opin Plant Biol., 8(3), 264-271. doi:https://doi.org/10.1016/j.pbi.2005.03.002
20. Kolm, R.H., Danielson, U.H., Zhang, Y., Talalay, P., Mannervik, B. (1995). Isothiocyanates as substrates for human glutathione transferases: structure-activity studies. Biochemistry Journal, 311(2), 453-459. doi:https://doi.org/10.1042/bj3110453
21. Uda, Y., Kurata, T., Arakawa, N. (1986). Effects of pH and ferrous ion on the degradation of glucosinolates by myrosinase. Agr Bio Chem, 50(11), 27352740. doi:https://doi.org/10.1271/bbb1961.50.2735
22. Hasapıs, X., MacLeod, A.J. (1982). Benzylglucosinolate degradation in heat-treated Lepidium sativum seeds and detection of a thiocyanate- forming factor. Phytochemistry, 21(5), 1009–1013. doi:https://doi.org/10.1016/S0031-9422(00)82405-X
23. Burow, M., Bergner, A., Gershenzon, J., Wıttstock, U. (2007). Glucosinolate Hydrolysis İn Lepidium sativum İdentification Of the Thiocyanate-Forming Protein. Plant Mol Biol., 63(1), 49–61. doi:https://doi.org/10.1007/s11103-006-9071-5
24. Thangstad, O.P., Winge, P., Husebye, H., Bones, A. (1993). The myrosinase gene family in Brassicaceae. Plant Mol Biol., 23(3), 511-524. doi:https://doi.org/10.1007/BF00019299
25. Rask, L., Anderson, E., Ekbom, B., Eriksson, S., Pontoppidan, B., Meijer, J. (2000). Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol Biol, 42(1), 93-113. doi:https://doi.org/10.1023/A:1006380021658
26. Mccully, M., Miller, C., Sprague, S. (2008). The distribution of glucosinolates and sulfur-rich cells in roots of field-grown canola Brassica napus. New. Phytol., 180(1), 193-205. doi:https://doi.org/10.1111/j.1469-8137.2008.02520.x
27. Ishimoto, H., Fukushi, Y., Yoshida, T., Tahara, S. (2000). Rhizopus and Fusarium are selected as dominant fungal genera in rhizospheres of Brassicaceae. J Chem Ecol., 26(10), 2387-2399. doi:https://doi.org/10.1023/A:1005583012561
28. Tierens, K., Thomma, B.P.H., Brouwer, M., Schmidt, J., Kistner, K., Porzel, A., Mauch-Mani, B., Cammue, B.P.A., Broekaert, W.F. (2001). Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens. Plant Physiol, 125(4), 1688-1699. doi:https://doi.org/10.1104/pp.125.4.1688
29. Mithen, R.F., Lewis, BG., Fenwick, G.R. (1986). In vitro activity of glucosinolates and their products against Leptosphaeria maculans. Transactions of the British Mycological Society, 87(3), 433-440. doi:https://doi.org/10.1016/S0007-1536(86)80219-4
30. Kawakishi, S., Kaneko, T. (1985). Interaction of oxidized glutathione with allyl isothiocyanate. Phytochemistry, 24(4): 715-718. doi:https://doi.org/10.1016/S0031-9422(00)84882-7
31. Kliebenstein, D.J., Figuth, A. and Mitchell-Olds, T., (2002). Genetic architecture of plastic methyl jasmonate responses in Arabidopsis thaliana. Genetics, 161(4),1685-1696
32. Wu, X., Meijer, M.J. (1999.) In Vitro Degradation of intact glucosinolates by phytopathogenic fungi of Brassica. Proceedings of the 10th International Rapeseed Congress, Canberra, Australia.
33. Brader, G., Mikkelsen, M.D., Halkier, B.A., TapioPalva, E. (2006). Altering glucosinolate profiles modulates disease resistance in plants. The Plant Journal, 46(5), 758-767. doi:https://doi.org/10.1111/j.1365-313X.2006.02743.x
34. Calmes, B., Guyen, G., Dumur, J., Brisach, C.A., Campio, C., Iacomi, B., Pigne, S., Dias, E., Macherel, D., Guillemette, T., Simoneau, P. (2015). Glucosinolate-derived isothiocyanates impact mitochondrial function in fungal cells and elicit an oxidative stress response necessary for growth recovery. Frontiers in the plant. Science, (6), Article 414. doi:https://doi.org/10.3389/fpls.2015.00414
35. Mueller, C., Agerbirk, N., Olsen, C.E., Boeve, J.L., Schaffner, U., Brakefield, P.M. (2001). Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athaliarosae. J Chem Ecol., 27(12), 2505-2516. doi:https://doi.org/10.1023/A:1013631616141
36. Jones, A.M.E., Winge, P., Bones, A.M., Cole, R., Rossiter, J.T. (2002). Characterization and evolution of a myrosinase from the cabbage aphid Brevicoryne brassicae. Insect Biochem Mol Biol, 32(3), 275-284. doi:https://doi.org/10.1016/s0965-1748(01)00088-1
37. Seifbarghi, S., Borhan, M. H., Wei, Y., Coutu, C., Robinson, S. J., & Hegedus, D. D. (2017). Changes in the Sclerotinia sclerotiorum transcriptome during infection of Brassica napus. BMC Genomic, 18(1), 266. doi:https://doi.org/10.1186/s12864-017-3642-5
38. Ratzka, A., Vogel, H., Kliebenstein, D.J., Mitchell-Olds, T., Kroymann, J. (2002). Disarming the mustard oil bomb. PNAS, 99(17), 11223-11228. doi:https://doi.org/10.1073/pnas.172112899
39. Wittstock, U., Agerbirk, N., Stauber, E.J., Olsen, C.E., Hippler, M., Mitchell-Olds, T., Gershenzon, J., Vogel, H. (2004). Successful herbivore attacks due to metabolic diversion of a plant chemical defense. Proc Natl Acad Sci USA, 101(14), 4859-4864. doi:https://doi.org/10.1073/pnas.0308007101
40. Agrawal, A.A., and Kurashige, N.S., (2003). A role for isothiocyanates in plant resistance against the specialist herbivore Pieris rapae. J Chem Ecol., 29(6), 1403-1415. doi:https://doi.org/10.1023/A:1024265420375
41. Van Poecke, R.M., Posthumus, M.A., Dicke, M. (2001). Herbivore-induced volatile production by Arabidopsis thaliana leads to the attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis. J Chem Ecol., 27(10), 1911-1928. doi:https://doi.org/10.1023/A:1012213116515
42. Sexton, A.C., Kirkgaard, J.A., Howlett, B.J. (1999). Glucosinolates in Brassica juncea and resistance to Australian isolates of Leptosphaeria maculans, the blackleg fungus. Australian Plant Pathology, 28(2), 95-102. doi:https://doi.org/10.1071/AP99017
43. Pedras, M.S.C., P. Ahianhonu, W.K., Hossain, M. (2004). Detoxification of the cruciferous phytoalexin brassinin in Sclerotinia sclerotiorum requires an inducible glucosyltransferase. Phytochemistry, 65(19), 2685-2694. doi:https://doi.org/10.1016/j.phytochem.2004.08.033
44. Rabot, S., Guerin, C., Nugon-Baudon, L., Szylit, O. (1995). Glucosinolate degradation by bacterial strains isolated from a human intestinal microflora. Proc.9th Int. Rapeseed Congress, Cambridge. B, 26, 212-214.
45. Rahmanpour, S. (2008). Studies on the role of the glucosinolate-myrosinase system resistance of oilseed rape to Sclerotinia sclerotiorum, Ph.D. Thesis, University of New England, Australia.116 pp.
46. Manici, L. M., Lazzeri, L., Palmieri, S. (1997). In vitro fungitoxic activity of some glucosinolates and their enzyme-derived products toward plant pathogenic fungi. Journal of Agricultural and Food Chemistry, 45(7), 2768-2773. doi:https://doi.org/10.1021/jf9608635
47. Sellam, A., P Poupard., -Simoneau, P. (2006). Molecular cloning ofAbGst1 encoding a glutathione transferase differentially expressed during exposure of Alternaria brassicicola to isothiocyanates. FEMS Microbiology Letters, 258, 241-249. doi:https://doi.org/10.1111/j.1574-6968.2006.00223.x
48. Francis, F., Vanhaelen, N., Haubruge, E. (2005). Glutathione S-transferases in the adaptation to plant secondary metabolites in the Myzus persicae aphid. Archives of Insect Biochemistry and Physiology, 58(3), 166-174. doi: https://doi.org/10.1002/arch.20049
49. Kim, J.H. and Jander, G., (2007). Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. The Plant Journal, 49(6), 1008-1019. doi:https://doi.org/10.1111/j.1365-313X.2006.03019.x