Jasmonate-mediated induced volatiles in the American cranberry, Vaccinium macrocarpon: From gene expression to organismal interactions

Frontiers in Plant Science

Volumn 4, Issue APR, 2013, Pages

  Rodriguez Saona, Cesar R ^a   Polashock, James ^a   Malo, Edi A ^b  

^a RUTGERS UNIVERSITY   (United States)

^b EL COLEGIO DE LA FRONTERA SUR   (Mexico)

Author keywords

Electroantennograms; Herbivore induced plant volatiles; Jasmonic acid; Methyl jasmonate; Multi trophic interactions; Sparganothis sulfureana

Indexed keywords

EID: 84900852865     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00115     Document Type: Article

References (80)

1. Abe, H., Shimoda, T., Ohnishi, J., Kugimiya, S., Narusaka, M., Seo, S., et al. (2009). Jasmonate-dependent plant defense restricts thrips performance and preference. BMC Plant Biol. 9:97. doi:10.1186/1471-2229-9-97
2. Agrawal, A. A. (1998). Induced responses to herbivory and increased plant performance. Science 279, 1201-1202.
3. Agrawal, A. A. (2000). Benefits and costs of induced plant defense for Lepidium virginicum (Brassicaceae). Ecology 81, 1804-1813.
4. Alborn, H. T., Turlings, T. C. J., Jones, T. H., Stenhagen, G., Loughrin, J. H., and Tumlinson, J. H. (1997). An elicitor of plant volatiles from beet armyworm oral secretion. Science 276, 945-949.
5. Arimura, G.-I., Kost, C., and Boland, W. (2005). Herbivore-induced, indirect plant defences. Biochim. Biophys. Acta 1734, 91-111.
6. Averill, A. L., and Sylvia, M. M. (1998). Cranberry Insects of the Northeast. Amherst: University of Massachusetts Extension.
7. Baldwin, I. T. (1998). Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc. Natl. Acad. Sci. U.S.A. 95, 8113-8118.
8. Ballhorn, D. J., Kautz, S., and Heil, M. (2013). Distance and sex determine host plant choice by herbivorous beetles. PLoS ONE 8:e55602. doi:10.1371/journal.pone.0055602
9. Bartram, S., Jux, A., Gleixner, G., and Boland, W. (2006). Dynamic pathway allocation in early terpenoid biosynthesis of stress-induced lima bean leaves. Phytochemistry 67, 1661-1672.
10. Bates, D., Maechler, M., and Bolker, B. (2011). lme4: Linear Mixed-effects Models Using S4 Classes. R Package Version 0.999375-42. Available at: http://CRAN.R-project.org/package=lme4.
11. Beckwith, C. S. (1938). Sparganothis sulfureana Clem., a cranberry pest in New Jersey. J. Econ. Entomol. 31, 253-256.
12. Bell, R. A., Owens, C. D., Shapiro, M., and Tardiff, J. R. (1981). "Development of mass rearing technology, " in The Gypsy Moth: Research Toward Integrated Pest Management, eds C. C. Doane and M. L. McManus (Washington: US Department of Agricultural), 599-633.
13. Birkett, M. A., Campbell, C. A. M., Chamberlain, K., Guerrieri, E., Hick, A. J., Martin, J. L., et al. (2000). New roles for cis-jasmone as an insect semiochemical and in plant defense. Proc. Natl. Acad. Sci. U.S.A. 97, 9329-9334.
14. Boland, W., Gäbler, A., Gilbert, M., and Feng, Z. (1998). Biosynthesis of C11 and C16 homoterpenes in higher plants; stereochemistry of the C-C-bond cleavage reaction. Tetrahedron 54, 14725-14736.
15. Boughton, A. J., Hoover, K., and Felton, G. W. (2006). Impact of chemical elicitor applications on greenhouse tomato plants and population growth of the green peach aphid, Myzus persicae. Entomol. Exp. Appl. 120, 175-188.
16. Bruinsma, M., Ijdema, H., Van Loon, J. J. A., and Dicke, M. (2008). Differential effects of jasmonic acid treatment of Brassica nigra on the attraction of pollinators, parasitoids, and butterflies. Entomol. Exp. Appl. 128, 109-116.
17. Bruinsma, M., Posthumus, M. A., Mumm, R., Mueller, M. J., Van Loon, J. J. A., and Dicke, M. (2009). Jasmonic acid-induced volatiles of Brassica oleracea attract parasitoids: effects of time and dose, and comparison with induction by herbivores. J. Exp. Bot. 60, 2575-2587.
18. Bruinsma, M., Van Dam, N. M., Van Loon, J. J., and Dicke, M. (2007). Jasmonic acid-induced changes in Brassica oleracea affect oviposition preference of two specialist herbivores. J. Chem. Ecol. 33, 655-668.
19. Chehab, E. W., Kaspi, R., Savchenko, T., Rowe, H., Negre-Zakharov, F., Kliebenstein, D., et al. (2008). Distinct roles of jasmonates and aldehydes in plant-defense responses. PLoS ONE 3:e1904. doi:10.1371/journal.pone.0001904
20. Cipollini, D. Jr., and Redman, A. (1999). Age-dependent effects of jasmonic acid treatment and wind exposure on foliar oxidase activity and insect resistance in tomato. J. Chem. Ecol. 25, 271-281.
21. Cipollini, D., Purrington, C. B., and Bergelson, J. (2003). Costs of induced responses in plants. Basic Appl. Ecol. 4, 79-89.
22. Cooper, W. R., and Goggin, F. L. (2005). Effects of jasmonate-induced defenses in tomato on the potato aphid, Macrosiphum euphorbiae. Entomol. Exp. Appl. 115, 107-115.
23. De Moraes, C. M., Mescher, M. C., and Tumlinson, J. H. (2001). Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410, 577-580.
24. Denno, R. F., Peterson, M. A., Gratton, C., Cheng, J., Langellotto, G. A., Huberty, A. F., et al. (2000). Feeding-induced changes in plant quality mediate interspecific competition between sap-feeding herbivores. Ecology 81, 1814-1827.
25. Dicke, M., Gols, R., Ludeking, D., and Posthumus, M. (1999). Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants. J. Chem. Ecol. 25, 1907-1922.
26. Dicke, M., and Vet, L. E. M. (1999). "Plant-carnivore interactions: evolutionary and ecological consequences for plant, herbivore and carnivore, " in Herbivores: Between Plants and Predators, eds H. Olff, V. K. Brown, and R. H. Drent (Oxford: Blackwell Science Ltd), 483-520.
27. Dudareva, N., Klempien, A., Muhlemann, J. K., and Kaplan, I. (2013). Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol. 198, 16-32.
28. Erbilgin, N., Krokene, P., Christiansen, E., Zeneli, G., and Gershenzon, J. (2006). Exogenous application of methyl jasmonate elicits defenses in norway spruce (Picea abies) and reduces host colonization by the bark beetle Ips typographus. Oecologia 148, 426-436.
29. Farmer, E. E., Johnson, R. R., and Ryan, C. A. (1992). Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiol. 98, 995-1002.
30. Felton, G. W., and Korth, K. L. (2000). Trade-offs between pathogen and herbivore resistance. Curr. Opin. Plant Biol. 3, 309-314.
31. Georgi, L., Johnson-Cicalese, J., Honig, J., Das, S. P., Rajah, V. D., Bhattacharya, D., et al. (2013). The first genetic map of the American cranberry: exploration of synteny conservation and quantitative trait loci. Theor. Appl. Genet. 126, 673-692.
32. Gols, R., Posthumus, M. A., and Dicke, M. (1999). Jasmonic acid induces the production of gerbera volatiles that attract the biological control agent Phytoseiulus persimilis. Entomol. Exp. Appl. 93, 77-86.
33. Gols, R., Roosjen, M., Dijkman, H., and Dicke, M. (2003). Induction of direct and indirect plant responses by jasmonic acid, low spider mite densities, or a combination of jasmonic acid treatment and spider mite infestation. J. Chem. Ecol. 29, 2651-2666.
34. Hare, J. D. (2007). Variation in herbivore and methyl jasmonate-induced volatiles among genetic lines of Datura wrightii. J. Chem. Ecol. 33, 2028-2043.
35. Hare, J. D. (2011). Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu. Rev. Entomol. 56, 161-180.
36. Heil, M. (2004). Induction of two indirect defences benefits lima bean (Phaseolus lunatus, fabaceae) in nature. J. Ecol. 92, 527-536.
37. Heil, M. (2010). Plastic defence expression in plants. Evol. Ecol. 24, 555-569.
38. Hothorn, T., Bretz, F., and Westfall, P. (2008). Simultaneous inference in general parametric models. Biometr. J. 50, 346-363.
39. Karban, R., and Baldwin, I. T. (1997). Induced Responses to Herbivory. Chicago: University of Chicago Press.
40. Kessler, A., and Baldwin, I. T. (2001). Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 2141-2144.
41. Lichtenthaler, H. K., Rohmer, M., and Schwender, J. (1997). Two independent biochemical pathways for isopentenyl diphosphate and isoprenoid biosynthesis in higher plants. Physiol. Plant. 101, 643-652.
42. Lu, Y.-B., Liu, S.-S., Liu, Y.-Q., Furlong, M. J., and Zalucki, M. P. (2004). Contrary effects of jasmonate treatment of two closely related plant species on attraction of and oviposition by a specialist herbivore. Ecol. Lett. 7, 337-345.
43. Malo, E. A., Castrejón-Gómez, V. R., Cruz-López, L., and Rojas, J. C. (2004). Antennal 20 sensilla and electrophysiological response of male and female Spodoptera frugiperda 21 (Lepidoptera: Noctuidae) to conspecific sex pheromone and plant odors. Ann. Entomol. Soc. Am. 97, 1273-1284.
44. McCallum, E. J., Cunningham, J. P., Lucker, J., Zalucki, M. P., De Voss, J. J., and Botella, J. R. (2011). Increased plant volatile production affects oviposition, but not larval development, in the moth Helicoverpa armigera. J. Exp. Biol. 214, 3672-3677.
45. Meng, Z. J., Yan, S. C., Yang, C. P., Jin, H., and Hu, X. O. (2011). Behavioural responses of Dendrolimus superans and Anastatus japonicus to chemical defences induced by application of jasmonic acid on larch seedlings. Scand. J. Forest Res 26, 53-60.
46. Omer, A. D., Granett, J., Karban, R., and Villa, E. M. (2001). Chemically-induced resistance against multiple pests in cotton. Int. J. Pest Manag. 47, 49-54.
47. Omer, A. D., Thaler, J. S., Granett, J., and Karban, R. (2000). Jasmonic acid induced resistance in grapevines to a root and leaf feeder. J. Econ. Entomol. 93, 840-845.
48. Ozawa, R., Shiojiri, K., Sabelis, M. W., Arimura, G., Nishioka, T., and Takabayashi, J. (2004). Corn plants treated with jasmonic acid attract more specialist parasitoids, thereby increasing parasitization of the common armyworm. J. Chem. Ecol. 30, 1797-1808.
49. Paré, P. W., and Tumlinson, J. H. (1999). Plant volatiles as a defense against insect herbivores. Plant Physiol. 121, 325-332.
50. Price, P. W., Bouton, C. E., Gross, P., McPheron, B. A., Thompson, J. N., and Weis, A. E. (1980). Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11, 41-65.
51. R Development Core Team. (2012). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. ISBN 3-900051-07-0. Available at: URL http://www.R-project.org/
52. Raguso, R. A., Levin, R. A., Foose, S. E., Holmberg, M. W., and McDade, L. A. (2003). Fragrance chemistry, nocturnal rhythms and pollination 'syndromes' in Nicotiana. Phytochemistry 63, 265-284.
53. Rodriguez-Saona, C. (2011). Herbivore-induced blueberry volatiles and intra-plant signaling. J. Vis. Exp. 58, e3440.
54. Rodriguez-Saona, C., Blaauw, D. R., and Isaacs, R. (2012). "Manipulation of natural enemies in agroecosystems: Habitat and semiochemicals for sustainable insect pest control, " in Integrated Pest Management and Pest Control-Current and Future Tactics, eds M. L. Larramendy and S. Soloneski (Rijeka: In Tech), 89-126.
55. Rodriguez-Saona, C., Crafts-Brandner, S. J., Paré, P. W., and Henneberry, T. J. (2001). Exogenous methyl jasmonate induces volatile emissions in cotton plants. J. Chem. Ecol. 27, 679-695.
56. Rodriguez-Saona, C., Poland, T. M., Miller, J. R., Stelinski, L. L., Grant, G. G., De Groot, P., et al. (2006). Behavioral and electrophysiological responses of the emerald ash borer, Agrilus planipennis, to induced volatiles of Manchurian ash, Fraxinus mandshurica. Chemoecology 16, 75-86.
57. Rodriguez-Saona, C., Vorsa, N., Singh, A., Johnson-Cicalese, J., Szendrei, Z., Mescher, M., et al. (2011). Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences. J. Exp. Bot. 62, 2633-2644.
58. Rohwer, C. L., and Erwin, J. E. (2008). Horticultural applications of jasmonates: a review. J. Hortic. Sci. Biotech. 83, 283-304.
59. Rohwer, C. L., and Erwin, J. E. (2010). Spider mites (Tetranychus urticae) perform poorly on and disperse from plants exposed to methyl jasmonate. Entomol. Exp. Appl. 137, 143-152.
60. Scheiner, S. M. (2001). "MANOVA: multiple response variables and multispecies interactions, " in Design and Analysis of Ecological Experiments, 2nd Edn, eds S. M. Scheiner and J. Gurevitch (New York: Oxford University Press), 99-155.
61. Schmelz, E. A., Alborn, H. T., and Tumlinson, J. H. (2003). Synergistic interactions between volicitin, jasmonic acid and ethylene mediate insect-induced volatile emission in Zea mays. Physiol. Plant. 117, 403-412.
62. Senthil-Nathan, S., Kalaivani, K., Choi, M.-Y., and Paik, C.-H. (2009). Effects of jasmonic acid-induced resistance in rice on the plant brownhopper, Nilaparvata lugens Stål (Homoptera: Delphacidae). Pestic. Biochem. Physiol. 95, 77-84.
63. Staswick, P. E., and Lehman, C. C. (1999). "Jasmonic acid-signaled responses in plants, " in Inducible Plant Defenses Against Pathogens and Herbivores: Biochemistry, Ecology, and Agriculture, eds A. A. Agrawal, S. Tuzun, and E. Bent (St. Paul: APS Press), 117-136.
64. Suckling, D. M., Karg, G., Gibb, A. R., and Bradley, S. J. (1996). Electroantennogram and oviposition responses of Epiphyas postvittana (Lepidoptera: Tortricidae) to plant volatiles. New Zeal. J. Crop Hort. Sci. 24, 323-333.
65. Tan, C.-W., Chiang, S.-Y., Ravuiwasa, K., Yadav, J., and Hwang, S.-Y. (2012). Jasmonate-induced defenses in tomato against Helicoverpa armigera depend in part on nutrient availability, but artificial induction via methyl jasmonate does not. Arthropod Plant Interact 6, 531-541.
66. Thaler, J., Stout, M., Karban, R., and Duffey, S. (1996). Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J. Chem. Ecol. 22, 1767-1781.
67. Thaler, J. S. (1999a). "Jasmonic acid mediated interactions between plants, herbivores, parasitoids, and pathogens: a review of field experiments in tomato, " in Inducible Plant Defenses Against Pathogens and Herbivores: Biochemistry, Ecology, and Agriculture, eds A. A. Agrawal, S. Tuzun, and E. Bent (St. Paul: APS Press), 319-334.
68. Thaler, J. S. (1999b). Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399, 686-688.
69. Thaler, J. S. (1999c). Induced resistance in agricultural crops: effects of jasmonic acid on herbivory and yield in tomato plants. Environ. Entomol. 28, 30-37.
70. Thaler, J. S. (2002). Effect of jasmonate-induced plant responses on the natural enemies of herbivores. J. Anim. Ecol. 71, 141-150.
71. Thaler, J. S., Stout, M. J., Karban, R., and Duffey, S. S. (2001). Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol. Entomol. 26, 312-324.
72. Tholl, D., and Röse, U. S. R. (2006). "Detection and identification of floral scent compounds, " in Biology of Floral Scent, eds N. Dudareva and E. Pichersky (Boca Raton: CRC Press), 3-25.
73. Turlings, T. C. J., Tumlinson, J. H., and Lewis, W. J. (1990). Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250, 1251-1253.
74. van Poecke, R. M. P., and Dicke, M. (2002). Induced parasitoid attraction by Arabidopsis thaliana: involvement of the octadecanoid and the salicylic acid pathway. J. Exp. Bot. 53, 1793-1799.
75. Van Zandt, P. A., and Agrawal, A. A. (2004). Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85, 2616-2629.
76. Vet, L. E. M., and Dicke, M. (1992). Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37, 141-172.
77. Viswanathan, D. V., Narwani, A. J. T., and Thaler, J. S. (2005). Specificity in induced plant responses shapes patterns of herbivore occurrence on Solanum dulcamara. Ecology 86, 886-896.
78. Walling, L. L. (2000). The myriad plant responses to herbivores. J. Plant Growth Regul. 19, 195-216.
79. Warabieda, W., and Olszak, R. (2010). Effect of exogenous methyl jasmonate on numerical growth of the population of the two-spotted spider mite (Tetranychus urticae Koch.) on strawberry plants and young apple trees. J. Plant Protect. Res. 50, 541-544.
80. Zheng, S.-J., and Dicke, M. (2008). Ecological genomics of plant-insect interactions: from gene to community. Plant Physiol. 146, 812-817.