Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Tian, Donglan ^a   Peiffer, Michelle ^a   Shoemaker, Erica ^a   Tooker, John ^a   Haubruge, Eric ^b   Francis, Frederic ^b   Luthe, Dawn S ^a   Felton, Gary W ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE OXIDASE; JASMONIC ACID; PROTEINASE INHIBITOR; CYCLOPENTANE DERIVATIVE; OXYLIPIN; TELOMERIC REPEAT BINDING FACTOR 1; VEGETABLE PROTEIN;

ARMYWORM; ARTICLE; CATERPILLAR; CONTROLLED STUDY; EARLY RESPONSE GENE; GENE INDUCTION; NONHUMAN; PIN2 GENE; PLANT DEFENSE; PLANT GENE; PLANT IMMUNITY; PROTEIN ANALYSIS; PROTEOMICS; SALIVATION; SPECIES DIFFERENCE; TOMATO; TRICHOME; ANIMAL; ANTIBODY SPECIFICITY; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LEPIDOPTERA; METABOLISM; SALIVA; SECRETION; SIGNAL TRANSDUCTION; TIME; TRANSCRIPTION INITIATION;

HELICOVERPA ZEA; HELIOTHIS VIRESCENS; LYCOPERSICON ESCULENTUM; NICOTIANA TABACUM; NOCTUIDAE; SPODOPTERA EXIGUA;

ANIMALS; CYCLOPENTANES; GENE EXPRESSION REGULATION, PLANT; GLUCOSE OXIDASE; LEPIDOPTERA; LYCOPERSICON ESCULENTUM; ORGAN SPECIFICITY; OXYLIPINS; PLANT PROTEINS; PROTEOMICS; SALIVA; SIGNAL TRANSDUCTION; TELOMERIC REPEAT BINDING PROTEIN 1; TIME FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84860493606     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036168     Document Type: Article

References (95)

1. Kaloshian I, Walling LL, (2005) Hempiterans as plant pathogens. Annual Review of Phytopathology 43: 491-521.
2. Walling LL, (2000) The Myriad Plant Responses to Herbivores. Journal of Plant Growth Regulation 19: 195-216.
3. Leitner M, Boland W, Mithofer A, (2005) Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytologist 167: 597-606.
4. Arimura GI, Kost C, Boland W, (2005) Herbivore-induced, indirect plant defences. Biochim Biophysica Acta (BBA) - Molecular Cell Biology and Lipids 1734: 91-111.
5. Simmons AT, Gurr GM, McGrath D, Martin PM, Nicol HI, (2004) Entrapment of Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) on glandular trichomes of Lycopersicon species. Australian Journal of Entomology 43: 196-200.
6. Pautot V, Holzer FM, Reisch B, Walling LL, (1993) Leucine aminopeptidase: an inducible component of the defense response in Lycopersicon esculentum (tomato). Proceedings of the National Academy of Sciences USA 90: 9906-9910.
7. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, et al. (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448: 661-665.
8. Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA, (2008) From the Cover: COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proceedings of the National Academy of Sciences 105: 7100-7105.
9. Thaler J-S, Stout M-J, Karban R, Duffey S-S, (2001) Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecological Entomology.
10. Felton GW, (2005) Indigestion is a plant's best defense. Proceedings of the National Academy of Sciences 102: 18771-18772.
11. Lin L, Shen TC, Chen YH, Hwang SY, (2008) Responses of Helicoverpa armigera to tomato plants previously infected by ToMV or damaged by H. armigera. Journal of Chemical Ecology 34: 353-361.
12. Felton GW, Donato K, Delvecchio RJ, Duffey SS, (1989) Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. Journal of Chemical Ecology 15: 2667-2694.
13. Felton GW, Workman J, Duffey SS, (1992) Avoidance of antinutritive plant defense - role of midgut pH in Colorado potato beetle. Journal of Chemical Ecology 18: 571-583.
14. Constabel CP, Bergey DR, Ryan CA, (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proceedings of the National Academy of Sciences 92: 407-411.
15. Thipyapong P, Stout MJ, Attajarusit J, (2007) Functional analysis of Polyphenol Oxidases by Antisense/Sense technology. Molecules 12: 1569-1595.
16. Diez-Diaz M, Conejero V, Rodrigo I, Pearce G, Ryan CA, (2004) Isolation and characterization of wound-inducible carboxypeptidase inhibitor from tomato leaves. Phytochemistry 65: 1919-1924.
17. Felton G-W, Summers C-B, (1993) Potential role of ascorbate oxidase as a plant defense protein against insect herbivory. Journal of Chemical Ecology 19: 1553-1568.
18. Farmer EE, (2007) Plant biology: Jasmonate perception machines. Nature 448: 659-660.
19. Victoriano E, Gregório EA, (2002) Ultrastructure of the excretory duct in the silk gland of the sugarcane borer Diatraea saccharalis (Lepidoptera: Pyralidae). Arthropod Structure & Development 31: 15-21.
20. Howe GA, Lightner J, Browse J, Ryan CA, (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8: 2067-2077.
21. Gurr GM, McGrath D, (2002) Foliar pubescence and resistance to potato moth, Phthorimaea operculella, in Lycopersicon hirsutum. Entomologia Experimentalis et Applicata 103: 35-41.
22. Bassel GW, Zielinska E, Mullen RT, Bewley JD, (2004) Down-regulation of DELLA genes is not essential for germination of tomato, soybean, and Arabidopsis seeds. Plant Physiology 136: 2782-2789.
23. Li L, Zhao YF, McCaig BC, Wingerd BA, Wang JH, et al. (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16: 126-143.
24. Boughton AJ, Hoover K, Felton GW, (2005) Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersicon esculentum. Journal of Chemical Ecology 31: 2211-2216.
25. Howe G-A, Lightner J, Browse J, Ryan C-A, (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell.
26. Lightner J, Pearce G, Ryan CA, Browse J, (1993) Isolation of signaling mutants of tomato (Lycopersicon esculentum). Molecular Gene Genetics 241: 595-601.
27. Narvaez-Vasquez J, Ryan CA, (2004) The cellular localization of prosystemin: a functional role for phloem parenchyma in systemic wound signaling. Planta 218: 360-369.
28. Narvaez-Vasquez J, Pearce G, Ryan CA, (2005) The plant cell wall matrix harbors a precursor of defense signaling peptides. Proceedings of the National Academy of Sciences 102: 12974-12977.
29. Pearce G, Ryan CA, (2003) Systemic signaling in tomato plants for defense against herbivores - Isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene. Journal of Biological Chemistry 278: 30044-30050.
30. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, et al. (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666-671.
31. Doares SH, Narvaez-Vasquez J, Conconi A, Ryan CA, (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiology 108: 1741-1746.
32. Felton GW, Korth KL, Bi JL, Wesley SV, Huhman DV, et al. (1999) Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Current Biology 9: 317-320.
33. Thaler JS, Karban R, Ullman DE, Boege K, Bostock RM, (2002) Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131: 227-235.
34. Orozco-Cardenas ML, Ryan CA, (2002) Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiology 130: 487-493.
35. Thaler JS, Bostock RM, (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogens and insects. Ecology 85: 48-58.
36. Diaz J, ten Have A, van Kan JA, (2002) The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea. Plant Physiology 129: 1341-1351.
37. Taylor BH, Young RJ, Scheuring CF, (1993) Induction of a proteinase inhibitor II-class gene by auxin in tomato roots. Plant Molecular Biology 23: 1005-1014.
38. Campos ML, de Almeida M, Rossi ML, Martinelli AP, Litholdo CG, et al. (2009) Brassinosteroids interact negatively with jasmonates in the formation of anti-herbivory traits in tomato. Journal of Experimental Botany 60: 4346-4360.
39. Orozco-Cardenas M, Ryan CA, (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proceedings of the National Academy of Sciences 96: 6553-6557.
40. Orozco-Cardenas ML, Narvaez-Vasquez J, Ryan CA, (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13: 179-191.
41. Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, et al. (2002) Herbivory: caterpillar saliva beats plant defences. Nature 416: 599-600.
42. Eichenseer H, Murphy JB, Felton GW, (2002) Sequestration of host plant carotenoids in the larval tissues of Helicoverpa zea. Joruanl of Insect Physiology 48: 311-318.
43. Eichenseer H, Murphy JB, Felton GW, (2002) Sequestration of host plant carotenoids in the larval tissues of Helicoverpa zea. Journal of Insect Physiology 48: 311-318.
44. Liu F, Cui LW, Cox-Foster D, Felton GW, (2004) Characterization of a salivary lysozyme in larval Helicoverpa zea. Journal of Chemical Ecology 30: 2439-2457.
45. Mori N, Alborn HT, Teal PE, Tumlinson JH, (2001) Enzymatic decomposition of elicitors of plant volatiles in Heliothis virescens and Helicoverpa zea. Journal of Insect Physiology 47: 749-757.
46. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH, (2004) Airborne signals prime plants against insect herbivore attack. Proceedings of the National Academy of Sciences 101: 1781-1785.
47. Musser R-O, Cipollini D-E, Hum-Musser S-M, Williams S-A, Brown J-K, et al. (2005) Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in Solanaceous plants. Archives of Insect Biochemistry and Physiology 58: 127-137.
48. Vincent R, Nadeau D, (1983) A micromethod for the quantitation of cellular proteins in Percoll with the Coomassie brilliant blue dye-binding assay. Analytical Biochemistry 135: 355-362.
49. Old WM, Meyer-Arendt K, Aveline-Wolf L, Pierce KG, Mendoza A, et al. (2005) Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Molecular & Cellular Proteomics 4: 1487-1502.
50. Celorio-Mancera MdlP, Courtiade J, Muck A, Heckel DG, Musser RO, et al. (2011) Sialome of a generalist lepidopteran herbivore: identification of transcripts and proteins from Helicoverpa armigera labial salivary glands. Plos One 6: e26676.
51. Eichenseer H, Mathews MC, Bi JL, Murphy JB, Felton GW, (1999) Salivary glucose oxidase: multifunctional roles for Helicoverpa zea? Archives of Insect Biochemistry and Physiology 42: 99-109.
52. Ryan CA, (1990) Proteinase inhibitors in plants: genes for improving defenses against insects and pathogens. Annual Review of Phytopathology 28: 425-449.
53. Howe GA, (2004) Jasmonates as signals in the wound response. Journal of Plant Growth Regulation 23: 223-237.
54. Peiffer M, Felton GW, (2005) The host plant as a factor in the synthesis and secretion of salivary glucose oxidase in larval Helicoverpa zea. Archives Insect Biochemistry and Physiology 58: 106-113.
55. Jia Y, Martin GB, (1999) Rapid transcript accumulation of pathogenesis-related genes during an incompatible interaction in bacterial speck disease-resistant tomato plants. Plant Molecular Biology 40: 455-465.
56. Al-Ghazi Y, Bourot S, Arioli T, Dennis ES, Llewellyn DJ, (2009) Transcript Profiling During Fiber Development Identifies Pathways in Secondary Metabolism and Cell Wall Structure That May Contribute to Cotton Fiber Quality. Plant and Cell Physiology 50: 1364-1381.
57. Harmel N, Letocart E, Cherqui A, Giordanengo P, Mazzucchelli G, et al. (2008) Identification of aphid salivary proteins: a proteomic investigation of Myzus persicae. Insect Molecular Biology 17: 165-174.
58. Eichenseer H, Mathews MC, Powell JS, Felton GW, (2010) Survey of a salivary effector in caterpillars: glucose oxidase variation and correlation with host range. Journal of Chemical Ecology 36: 885-897.
59. Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, et al. (2002) Herbivory: Caterpillar saliva beats plant defences - A new weapon emerges in the evolutionary arms race between plants and herbivores. Nature 416: 599-600.
60. Diezel C, von Dahl CC, Gaquerel E, Baldwin IT, (2009) Different Lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiology 150: 1576-1586.
61. Bede J, Musser R, Felton G, Korth K, (2006) Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terpenoid biosynthesis. Plant Molecular Biology 60: 519-531.
62. Weech M-H, Chapleau M, Pan L, Ide C, Bede JC, (2008) Caterpillar saliva interferes with induced Arabidopsis thaliana defence responses via the systemic acquired resistance pathway. Journal of Experimental Botany 59: 2437-2448.
63. Vandenabeele S, Van Der Kelen K, Dat J, Gadjev I, Boonefaes T, et al. (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proceedings of the National Academy of Sciences 100: 16113-16118.
64. Vellosillo T, Vicente J, Kulasekaran S, Hamberg M, Castresana C, (2010) Emerging complexity in reactive oxygen species production and signaling during the response of plants to pathogens. Plant Physiology 154: 444-448.
65. Brooks DM, Bender CL, Kunkel BN, (2005) The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defences in Arabidopsis thaliana. Molecular Plant Pathology 6: 629-639.
66. Grant MR, Jones JDG, (2009) Hormone (dis) harmony moulds plant health and disease. Science 324: 750.
67. Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, et al. (2004) Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell 16: 616-628.
68. Traw MB, Dawson TE, (2002) Differential induction of trichomes by three herbivores of black mustard. Oecologia 131: 526-532.
69. Agrawal AA, (1999) Induced responses to herbivory in wild radish: effects on several herbivores and plant fitness. Ecology 80: 1713-1723.
70. Dalin P, Björkman C, (2003) Adult beetle grazing induces willow trichome defence against subsequent larval feeding. Oecologia 134: 112-118.
71. Björkman C, Dalin P, Ahrné K, (2008) Leaf trichome responses to herbivory in willows: induction, relaxation and costs. New Phytologist 179: 176-184.
72. Holeski LM, (2007) Within and between generation phenotypic plasticity in trichome density of Mimulus guttatus. Journal of Evolutionary Biology 20: 2092-2100.
73. Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, et al. (2012) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiology 158: 854-863.
74. Boller T, He SY, (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324: 742.
75. Jones JDG, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
76. Mithofer A, Boland W, (2008) Recognition of herbivory-associated molecular patterns. Plant Physiology 146: 825-831.
77. Bonaventure G, VanDoorn A, Baldwin IT, (2011) Herbivore-associated elicitors: FAC signaling and metabolism. Trends in Plant Science 16: 294-299.
78. Felton GW, (2008) Caterpillar secretions and induced plant responses, Ch. 18. In: Schaller A, editors. Induced Plant Resistance to Herbivory Berlin Springer Science pp. 369-387.
79. Delphia C, Mescher M, Felton GW, De Moraes CM, (2006) The role of insect-derived cues in eliciting indirect plant defenses in tobacco, Nicotiana tabacum. Plant Signaling and Behavior 1: 243-250.
80. Qu N, Schittko U, Baldwin IT, (2004) Consistency of Nicotiana attenuata's herbivore- and jasmonate-induced transcriptional responses in the allotetraploid species Nicotiana quadrivalvis and Nicotiana clevelandii. Plant Physiology 135: 539-548.
81. Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, et al. (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276: 945-949.
82. Rose USR, Tumlinson JH, (2005) Systemic induction of volatile release in cotton: How specific is the signal to herbivory? Planta 222: 327-335.
83. Chung SH, Felton GW, (2011) Specificity of induced resistance in tomato against specialist Lepidopteran and Coleopteran species. Journal of Chemical Ecology 37: 378-386.
84. Korth KL, Dixon RA, (1997) Evidence for chewing insect-specific molecular events distinct from a general wound response in leaves. Plant Physiology 115: 1299-1305.
85. Yoshinaga N, Aboshi T, Ishikawa C, Fukui M, Shimoda M, et al. (2007) Fatty acid amides, previously identified in caterpillars, found in the cricket Teleogryllus taiwanemma and fruit fly Drosophila melanogaster larvae. Journal of Chemical Ecology 33: 1376-1381.
86. Halitschke R, Gase K, Hui D, Schmidt DD, Baldwin IT, (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates. Plant Physiology 131: 1894-1902.
87. Schmidt DD, Voelckel C, Hartl M, Schmidt S, Baldwin IT, (2005) Specificity in Ecological Interactions. Attack from the Same Lepidopteran Herbivore Results in Species-Specific Transcriptional Responses in Two Solanaceous Host Plants. Plant Physiol 138: 1763-1773.
88. Alborn H, Brennan M, Tumlinson J, (2003) Differential activity and degradation of plant volatile elicitors in regurgitant of tobacco hornworm (Manduca sexta) larvae. Journal of Chemical Ecology 29: 1357-1372.
89. Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, et al. (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proceedings of the National Academy of Sciences 103: 8894-8899.
90. Lawrence SD, Novak NG, Blackburn MB, (2007) Inhibition of proteinase inhibitor transcripts by Leptinotarsa decemlineata regurgitant in Solanum lycopersicum. Journal of Chemical Ecology 33: 1041-1048.
91. Peiffer M, Felton GW, (2009) Do caterpillars secrete "oral secretions"? Journal of Chemical Ecology 35: 326-335.
92. Rotenberg D, Thompson TS, German TL, Willis DK, (2006) Methods for effective real-time RT-PCR analysis of virus-induced gene silencing. Journal of Virological Methods 138: 49-59.
93. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC(T) method. Methods 25: 402-408.
94. Tooker JF, De Moraes CM, (2005) Jasmonate in lepidopteran eggs and neonates. Journal of Chemical Ecology 31: 2753-2759.
95. Schmelz EA, Engelberth J, Alborn HT, O'Donnell P, Sammons M, et al. (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proceedings of the National Academy of Sciences 100: 10552-10557.