Caterpillar Labial Saliva Alters Tomato Plant Gene Expression

Journal of Chemical Ecology

Volumn 38, Issue 11, 2012, Pages 1387-1401

  Musser, Richard O ^a   Hum Musser, Sue M ^a   Lee, Henry K ^a   DesRochers, Brittany L ^a   Williams, Spencer A ^a   Vogel, Heiko ^b  

^a WESTERN ILLINOIS UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

Caterpillar saliva; Gene expression; Glucose oxidase; Herbivory; Plant defense

Indexed keywords

ARRAY; CATERPILLAR; ENZYME ACTIVITY; FRUIT; GENE EXPRESSION; GENETIC ANALYSIS; HERB; HERBIVORY; INHIBITOR; PHENOL; PLANT DEFENSE; SALIVA; WOUNDING;

HELICOVERPA ZEA; LYCOPERSICON ESCULENTUM;

EID: 84870542326     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-012-0198-3     Document Type: Article

References (73)

1. Adams, D. O. and Yang, S. F. 1979. Ethylene biosynthesis: Identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc. Natl. Acad. Sci. USA 76: 170-174.
2. Alba, R., Fei, Z., Payton, P., Liu, Y., Moore, S. L., Debbie, P., Cohn, J., D'Ascenzo, M., Gordon, J. S., Rose, J. K., Martin, G., Tanksley, S. D., Bouzayen, M., Jahn, M. M., and Giovannoni, J. 2004. ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. Plant J. 39: 697-714.
3. 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.
4. Alborn, H. T., Jones, T. H., Stenhagen, G. S., and Tumlinson, J. H. 2000. Identification and synthesis of volicitin and related components from beet armyworm oral secretions. J. Chem. Ecol. 26: 203-220.
5. Babic, B., Poisson, A., Darwish, S., Lacasse, J., Merkx-Jacques, M., Despland, E., and Bede, J. C. 2008. Influence of dietary nutritional composition on caterpillar salivary enzyme activity. J. Insect Physiol. 54: 286-296.
6. Bae, E.-K., Lee, H., Lee, J.-S., and Noh, E.-W. 2009. Differential expression of a poplar SK2-type dehydrin gene in response to various stresses. Biochem. Mol. Biol. Rep. 42: 439-443.
7. Bede, J. C., Musser, R. O., Felton, G. W., and Korth, K. L. 2006. Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzyme in terpenoid biosynthesis. Plant Mol. Biol. 60: 519-531.
8. Benjamini, Y. and Hochberg, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. 57: 289-300.
9. Borovskii, G. B., Stupnikova, I. V., Antipina, A. I., Vladimirova, S. V., and Voinikov, V. K. 2002. Accumulation of dehydrin-like proteins in the mitochondria of cereals in response to cold, freezing, drought and ABA treatment. BMC Plant Biol. 2: 5.
10. Bradford, M. M. 1976. A dye binding assay for protein. Anal. Biochem. 72: 248-254.
11. Broadway, R. M. and Duffey, S. S. 1986. The effect of dietary protein on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. J. Insect Physiol. 32: 673-680.
12. Celorio-Mancera, M. D. L. P., Courtiade, J., Muck, A., Heckel, D. G., Musser, R. O., and Vogel, H. 2011. Sialome of a generalist lepidopteran herbivore: identification of transcripts and proteins from helicoverpa armigera labial salivary glands. PLoS One 6: e26676.
13. Chen, H., Wilkerson, C. G., Kuchar, J. A., Phinney, B. S., and Howe, G. A. 2005. Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Plant Biol. 102: 19237-19242.
14. Chippendale, G. M. 1970. Metamorphic changes in fat body proteins of the southwestern corn borer Diatraea grandiosella. J. Insect Physiol. 16: 1057-1068.
15. Constabel, P., Bergey, D., and Ryan, C. 1995. Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc. Natl. Acad. Sci. USA 92: 407-411.
16. Darwish, S. A., Pan, L., Ide, C., and Bede, J. C. 2008. Caterpillar-specific gene expression in the legume, Medicago truncatula. Plant Mol. Biol. Rep. 26: 12-31.
17. Delphia, C. M., Mescher, M. C., Felton, G. W., and de Moraes, C. M. 2006. The role of insect-derived cues in eliciting indirect plant defenses in tobacco, Nicotiana tabacum. Plant Signal. Behav. 1: 243-250.
18. de Vos, M., van Osten, V. R., van Poecke, R. M., van Pelt, J. A., Pozo, M. J., Mueller, M. J., Buchala, A. J., Métraux, J. P., van Loon, L. C., Dicke, M., and Pieterse, C. M. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant Microbe Interact. 18: 923-937.
19. de Vos, M., van Zaanen, W., Koornneef, A., Korzelius, J. P., Dicke, M., van Loon, L. C., and Pieterse, C. M. J. 2006. Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol. 142: 352-363.
20. Diezel, C., von Dahl, C., Gaquerel, E., and Baldwin, I. T. 2009. Different Lepidopteran elicitors account for crosstalk in herbivory-induced phytohormone sgnaling. Plant Physiol. 150: 1576-1586.
21. Eichenseer, H., Mathews, M. C., Jian, L. B., Murphy, J. B., and Felton, G. W. 1999. Salivary glucose oxidase: multifunctional roles for Helicoverpa zea? Arch. Insect Biochem. Physiol. 42: 99-109.
22. Eichenseer, H., Mathews, M. C., Powell, J. S., and Felton, G. W. 2010. Survey of a salivary effector in caterpillars: glucose oxidase variation and correlation with host range. J. Chem. Ecol. 36: 885-897.
23. Felton, G. W. 2005. Indigestion is a plant's best defense. Proc. Natl. Acad. Sci. USA 102: 18771-18772.
24. Felton, G. W. and Eichenseer, H. 1999. Herbivore saliva and its effect on plant defense against herbivores and pathogens, pp. 390, in A. A. Agrawal, S. Tuzun, and E. Bent (eds.), Induced plant defenses against pathogens and herbivores. APS Press, St. Paul.
25. Gao, W. R., Wang, X. S., Liu, Q. Y., Peng, H., Chen, C., Li, J. G., Zhang, J. S., Hub, S. N., and Maa, H. 2008. Comparative analysis of ESTs in response to drought stress in chickpea (C. arietinum L.). Biochem. Biophys. Res. Commun. 376: 578-583.
26. Glazebrook, J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43: 205-227.
27. Gomez, S. K., Cox, M. M., Bede, J. C., Inoue, K., Alborn, H. T., Tumlinson, J. H., and Korth, K. L. 2005. Lepidopteran herbivory and oral factors induce transcripts encoding novel terpene synthases in Medicago truncatula. Arch. Insect Biochem. Physiol. 58: 114-127.
28. Graham, J., Pearce, G., Merryweather, J., Koiti, T., Ericsson, L., and Ryan, C. 1985. Wound-induced proteinase inhibitors from tomato leaves. J. Biol. Chem. 260: 6555-6560.
29. Green, T. R. and Ryan, C. A. 1972. Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175: 776-777.
30. Heiden, A. C., Hoffmann, T., Kahl, J., Klockow, D., Langebartels, C., Mehlhorn, H., Sandermann Jr., H., Schraudner, M., Schuh, G., and Wildt, J. 1999. Emission of volatile organic compounds from ozone-exposed plants. Ecol. Appl. 9: 1160-1167.
31. Hermsmeier, D., Schittko, U., and Baldwin, I. T. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs. Plant Physiol. 125: 683-700.
32. Howe, G. A. and Jander, G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59: 41-66.
33. Koornneef, A. and Pieterse, C. M. J. 2008. Cross talk in defense signaling. Plant Physiol. 146: 839-844.
34. Korth, K. L. 2003. Profiling plant responses to herbivorous insects. Genome Biol. 4(7): 221. 1-221. 4.
35. Korth, K. L. and Thompson, G. A. 2006. Chemical signals in plants: jasmonates and the role of insect-derived elicitors in responses to herbivores, pp. 259-278, in S. Tuzun and E. Bent (eds.), Multigenic and induced systemic resistance in plants. Springer Publishing, New York.
36. Lawrence, S. D., Novak, N. G., Ju, C. J.-T., and Cooke, J. E. K. 2008. Potato, Solanum tuberosum, defense against Colorado Potato Beetle, Leptinotarsa decemlineata (Say): microarray gene expression profiling of potato by Colorado Potato Beetle regurgitant treatment of wounded leaves. J. Chem. Ecol. 34: 1013-1025.
37. Lawrence, S. D. and Novak, N. G. 2004. Maize genes induced by herbivory and volicitin. J. Chem. Ecol. 30: 2543-2557.
38. Leon, J., Lawton, M. A., and Raskin, I. 1995. Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol. 108: 1673-1678.
39. Leon-Reyes, A., Spoel, S. H., de Lange, E. S., Abe, H., Kobayashi, M., Tsuda, S., Millenaar, F. F., Welschen, R. A. M., Ritsema, T., and Pieterse, C. M. J. 2009. Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol. 149: 1797-1809.
40. Lou, Y. and Baldwin, I. T. 2003. Manduca sexta recognition and resistance among allopolyploid Nicotiana host plants. Proc. Natl. Acad. Sci. 100: 14581-14586.
41. Liu, Y., Hoffman, N. E., and Yang, S. F. 1985. Promotion by ethylene of the capability to convert 1-aminocyclopropane-1-carboxylic acid to ethylene in preclimacteric tomato and cantelope fruits. Plant Physiol. 77: 407-411.
42. Maffei, M. E., Mithöfer, A., and Boland, W. 2007a. Insects feeding on plants: Rapid signals and responses precede the induction of phytochemical release. Phytochemistry 68: 2946-2959.
43. Maffei, M. E., Mithöfe, R. A., and Boland, W. 2007b. Before gene expression: early events in plant herbivore interactions. Trends Plant Sci. 12: 310-316.
44. Mattiacci, L., Dicke, M., and Posthumus, M. A. 1995. β-glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc. Natl. Acad. Sci. USA 92: 2036-2040.
45. Mithöfer, A. and Boland, W. 2008. Recognition of herbivory-associated molecular patterns. Plant Physiol. 146: 825-831.
46. Mithöfer, A., Wanner, G., and Boland, W. 2005. Effects of feeding Spodoptera littoralis on Lima Bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol. 137: 1160-1168.
47. Musser, R. O., Hum-Musser, S. M., Eichenseer, H., Peiffer, M., Ervin, G., Murphy, J. B., and Felton, G. W. 2002a. Caterpillar saliva beats plant defences: a new weapon emerges in the evolutionary arms race between plants and herbivores. Nature 416: 599-600.
48. Musser, R. O., Hum-Musser, S. M., Slaten-Bickford, S. E., Felton, G. W., and Gergerich, R. C. 2002b. Evidence that ribonuclease activity present in beetle regurgitant is found to stimulate virus resistance in plants. J. Chem. Ecol. 28: 1691-1696.
49. Musser, R. O., Cipollini, D. F., Hum-Musser, S. M., Williams, S. A., Brown, J. K., and Felton, G. W. 2005a. Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in Solanaceous plants. Arch. Insect Biochem. Physiol. 58: 128-137.
50. Musser, R. O., Kwon, H. S., Willams, S. A., White, C. J., Romano, M., Bradbury, S., Brown, J. K., and Felton, G. W. 2005b. Evidence that caterpillar labial saliva suppresses pathogencity of potential bacterial pathogens. Arch. Insect Biochem. Physiol. 58: 138-144.
51. Musser, R. O., Farmer, E. E., Peiffer, M., Williams, S. A., and Felton, G. W. 2006. Ablation of caterpillar labial salivary glands: technique for determining the role of saliva in insect-plant interactions. J. Chem. Ecol. 32: 981-992.
52. O'Donnell, P., Calvert, C., Atzorn, R., Wasternack, C., Leyser, H. M. O., and Bowles, D. J. 1996. Ethylene as a signal mediating the wound response of tomato plants. Science 274(5294): 1914-1917.
53. Orozco-Cárdenas, M. L., Narváez-Vásquez, J., and Ryan, C. A. 2001. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, methyl jasmonate. Plant Cell 13: 179-191.
54. Peiffer, M. and Felton, G. W. 2005. The host plant as a factor in the synthesis and secretion of salivary glucose oxidase in the larval Helicoverpa zea. Arch. Insect Biochem. Physiol. 58: 106-113.
55. Ralph, S., Oddy, C., Cooper, D., Yueh, H., Jancsik, S., Kolosova, N., Philippe, R. N., Aeschliman, D., White, R., Huber, D., Ritland, C. E., Benoit, F., Rigby, T., Nantel, A., Butterfield, Y. S. N., Kirkpatrick, R., Chun, E., Liu, J., Palmquist, D., Wynhoven, B., Stott, J., Yang, G., Barber, S., Holt, R. A., Siddiqui, A., Jones, S. J. M., Marra, M. A., Ellis, B. E., Douglas, C. J., Ritland, K., and Bohlmann, J. 2006a. Genomics of hybrid poplar (Populus trichocarpa x deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Mol. Ecol. 15: 1275-1297.
56. Ralph, S., Yueh, H., Friedmann, M., Aeschliman, D., Zeznik, J. A., Nelson, C. C., Butterfield, Y. S. N., Kirkpatrick, R., Liu, J., Jones, S. J. M., Marra, M. A., Douglas, C. J., Ritland, K., and Bohlmann, J. 2006b. Conifer defence against insects: microarray gene expression profiling of Sitka spruce (Picea sitchensis) induced by mechanical wounding or feeding by spruce budworms (Choristoneura occidentalis) or white pine weevils (Pissodes strobi) reveals large-scale changes of the host transcriptome. Plant Cell Environ. 29: 1545-1570.
57. Reymond, P., Bodenhausen, N., van Poecke, R., Krishnamurthy, V., Dicke, M., and Farmer, E. E. 2004. A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16: 3132-3147.
58. Reymond, P., Weber, H., Damond, M., and Farmer, E. E. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12: 707-719.
59. Richard, S., Morency, M.-J., Drevet, C., Jouanin, L., and Seguin, A. 2000. Isolation and characterization of a dehydrin gene from white spruce induced upon wounding, drought and cold stresses. Plant Mol. Biol. 43: 1-10.
60. Rodriguez-Saona, C. R., Musser, R. O., Vogel, H., Hum-Musser, S. M., and Thaler, J. S. 2010. Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J. Chem. Ecol. 36: 1043-1057.
61. Skibbe, M., Qu, N., Galis, I., and Baldwin, I. T. 2008. Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20: 1984-2000.
62. Schittko, U., Hermsmeier, D., and Baldwin, I. T. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. II. Accumulation of plant mRNA in response to insect-derived cues. Plant Physiol. 125: 701-710.
63. Schmelz, E. A., Engelberth, J., Alborn, H. T., Tumlinson III, J. A., and Teal, P. E. A. 2009. Phytohormone-based activity mapping of insect herbivore-produced elicitors. Proc. Natl. Acad. Sci. USA 106(2): 653-657.
64. Schmelz, E. A., Carroll, M. J., Leclere, S., Phipps, S. M., Meredith, J., Chourey, P. S., Alborn, H. T., and Teal, P. E. A. 2006. Fragments of ATP synthase mediate plant perception of insect attack. Proc. Natl. Acad. Sci. USA 103: 8894-8899.
65. Storey, J. D. and Tibshirani, R. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 100: 9440-9445.
66. Tian, D., Peiffer, M., Shoemaker, E., Tooker, J., Haubruge, E., Francis, F., Luthe, D. S., and Felton, G. W. 2012. Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant. PLoS One 7: e36168.
67. Thipyapong, P. and Steffens, J. 1997. Tomato polyphenol oxidase (differential response of the polyphenol oxidase F promoter to injuries and wound signals). Plant Physiol. 115: 409-418.
68. Townsend, J. P. 2003. Multifactorial experimental design and the transitivity of ratios withspotted DNA microarrays. BMC Genomics 4: 41.
69. Weech, M. H., Chapleau, M., Pan, L., Ide, C., and Bede, J. C. 2008. Caterpillar saliva interferes with induced Arabidopsis thaliana defense responses via the systemic acquired resistance pathway. J. Exp. Bot. 59: 2437-2448.
70. Yang, S. F. and Hoffman, N. E. 1984. Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35: 155-189.
71. Yeboah, N. A., Arahira, M., Nong, V. H., Zhang, D., Kadokura, K., Watanabe, A., and Fukawaza, C. 1998. A class III acidic endochitinase is specifically expressed in the developing seeds of Soybean (Glycine max (L.) Merr.). Plant Mol. Biol. 36: 407-415.
72. Zong, N. and Wang, C. 2004. Induction of nicotine in tobacco by herbivory and its relation to glucose oxidase activity in the labial gland of three noctuid caterpillars. Chin. Sci. Bull. 49: 1596-1601.
73. Zong, N. and Wang, C. 2007. Larval feeding induced defensive responses in tobacco: comparison of two sibling species of Helicoverpa with different diet breadths. Planta 226: 215-224.