Tomato Spotted Wilt Virus Benefits a Non-Vector Arthropod, Tetranychus Urticae, by Modulating Different Plant Responses in Tomato

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Nachappa, Punya ^a   Margolies, David C ^b   Nechols, James R ^b   Whitfield, Anna E ^b   Rotenberg, Dorith ^b  

^a INDIANA UNIVERSITY PURDUE UNIVERSITY FORT WAYNE   (United States)

^b KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; JASMONIC ACID; SALICYLIC ACID;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FERTILITY; GENE EXPRESSION; HOST RANGE; NONHUMAN; PLANT DEFENSE; PLANT RESPONSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TETRANYCHUS URTICAE; TOMATO; TOSPOVIRUS; TRANSCRIPTOMICS; UPREGULATION;

ANIMALS; CELL WALL; CYCLOPENTANES; DOWN-REGULATION; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; OXYLIPINS; PLANT DISEASES; TETRANYCHIDAE; TOSPOVIRUS; TRANSCRIPTOME;

EID: 84884225237     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075909     Document Type: Article

References (52)

1. Stout MJ, Thaler JS, Thomma BPHJ, (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu Rev Entomol 51: 663-689. doi:10.1146/annurev.ento.51.110104.151117. PubMed: 16332227.
2. Mauck KE, De Moraes CM, Mescher MC, (2010) Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proc Natl Acad Sci USA 107: 3600-3605. doi:10.1073/pnas.0907191107. PubMed: 20133719.
3. Fereres A, Lister RM, Araya JE, Foster JE, (1989) Development and reproduction of the English grain aphid (Homoptera:Aphididae) on wheat cultivars infected with Barley yellow dwarf virus. Environ Entomol 18: 388-393.
4. Eigenbrode SD, Ding H, Shiel P, Berger PH, (2002) Volatiles from potato plants infected with potato leafroll virus attracts and arrest the virus vector, Myzus persicae (Homoptera:Aphididae). Proc R Soc Lond B 269: 455-460. doi:10.1098/rspb.2001.1909.
5. Blua MJ, Perring TM, Madore MA, (1994) Plant virus-induced changes in aphid population development and temporal fluctuations in plant nutrients. J Chem Ecol 20: 691-707. doi:10.1007/BF02059607.
6. Guo J-Y, Ye G-Y, Dong S-Z, Liu S-S, (2010) An invasive whitefly feeding on a virus-infected plant increased its egg production and realized fecundity. PLOS ONE 5: e11713. doi:10.1371/journal.pone.0011713. PubMed: 20676356.
7. Maris PC, Joosten NN, Goldbach RW, Peters D, (2004) Tomato spotted wilt virus infection improves host suitability for its vector Frankliniella occidentalis. Phytopathology 94: 706-711. doi:10.1094/PHYTO.2004.94.7.706. PubMed: 18943902.
8. Carter W, (1939) Populations of Thrips tabaci, with special reference to virus transmission. J Anim Ecol 8: 261-276. doi:10.2307/1234.
9. Belliure B, Janssen A, Maris PC, Peters D, Sabelis MW, (2005) Herbivore arthropods benefit from vectoring plant viruses. Ecol Lett 8: 70-79.
10. Abe H, Tomitaka Y, Shimoda T, Seo S, Sakurai T, et al. (2012) Antagonistic plant defense system regulated by phytohormones assists interactions among vector insect, thrips and a Tospovirus. Plant Cell Physiol 53: 204-212. doi:10.1093/pcp/pcr173. PubMed: 22180600.
11. Hare JD, Dodds JA, (1987) Survival of the Colorado potato beetle on virus-infected tomato in relation to plant nitrogen and alkaloid content. Entomol Exp Applicata 44: 31-35. doi:10.1111/j.1570-7458.1987.tb02236.x.
12. Thaler JS, Agrawal AA, Halitschke R, (2010) Salicylate-mediated interactions between pathogens and herbivores. Ecology 91: 1075-1082. doi:10.1890/08-2347.1. PubMed: 20462121.
13. Belliure B, Sabelis MW, Janssen A, (2010) Vector and virus induce plant responses that benefit a non-vector herbivore. Basic Appl Ecol 11: 162-169. doi:10.1016/j.baae.2009.09.004.
14. Pan H, Chen G, Li F, Wu Q, Wang S, et al. (2013) Tomato spotted wilt virus infection reduces the fitness of a nonvector herbivore on pepper. J Econ Entomol 106: 924-928. doi:10.1603/EC12365. PubMed: 23786083.
15. Walling LL, (2000) The myraid of plant responses to herbivores. J Plant Growth Regul 19: 195-216. PubMed: 11038228.
16. Glazebrook J, (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43: 205-227. doi:10.1146/annurev.phyto.43.040204.135923. PubMed: 16078883.
17. Thaler JS, Fidantsef AL, Duffey SS, Bostock RM, (1999) Tradeoffs in plant defense against pathogens and herbivores: a field demonstration using chemical elicitors of induced resistance. J Chem Ecol 25: 1597-1609. doi:10.1023/A:1020840900595.
18. Pena-cortes H, Albrecht T, Prat S, Weiler EW, Willmitzer L, (1993) Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191: 123-128.
19. Felton GW, Korth KL, (2000) Trade-offs between pathogen and herbviore resistance. Curr Opin Plant Biol 3: 309-314. doi:10.1016/S1369-5266(00)00086-8. PubMed: 10873851.
20. Doares SH, Narvaez-Vasquez J, Conconi A, Ryan CA, (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in toamto leaves induced by systemin and jasmonic acid. Plant Physiol 108: 1741-1746. PubMed: 12228577.
21. Bostock RM, (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43: 545-580. doi:10.1146/annurev.phyto.41.052002.095505. PubMed: 16078895.
22. Preston CA, Lewandowski C, Enyedi AJ, Baldwin IT, (1999) Tobacco mosaic virus inoculation inhibits wound-induced jasmonic acid-mediated responses within but not between plants. Planta 209: 87-95. doi:10.1007/s004250050609. PubMed: 10467034.
23. Markkula M, Laurema S, (1964) Changes in the concentration of free amino acids in plants induced by virus disease and the reproduction of aphids. Ann Agric Fenn 3: 265-271.
24. Hammond AM, Hardy TN, (1988) Quality of diseased plants as hosts for insects. In: Heinrichs EA, eds. Plant Stress-Insect Interactions. New York: Wiley. pp. pp. 657-672.
25. Yudin LS, Mitchell WC, Cho JJ, (1987) Color preference of thrips (Thysanoptera:Thripidae) with reference to aphids (Homoptera: Aphididae) and leafminers in Hawaiian lettuce farms. J Econ Entomol 80: 51-55.
26. German TL, Ullman DE, Moyer JW, (1992) Tospoviruses-diagnosis, molecular-biology, phylogeny, and vector relationships. Annu Rev Phytopathol, 30: 315-348. PubMed: 18643773.
27. Sherwood JL, German TL, Whitfield AE, Moyer JW, Ullman DE, (2001) Tospoviruses. In: Maloy OC, Murray TD, eds. Encyclopedia of Plant Pathology. New York: John Wiley & Sons Inc. pp. pp. 1034-1040.
28. Whitfield AE, Ullman DE, German TL, (2005) Tospovirus-thrips interactions. Annu Rev Phytopathol 43: 459-489. doi:10.1146/annurev.phyto.43.040204.140017. PubMed: 16078892.
29. van de Vrie M, McMurtry JA, Huffaker CB, (1972) Ecology of tetranychid mites and their natural enemies: a review. III. Biology, ecology and pest status, and host-plant relations of Tetranychids. Hilgardia 41: 343-432.
30. Nault BA, Speese J III, (2002) Major insect pests and economics of fresh-market tomato in eastern Virginia. Crop Protect 21: 359-366. doi:10.1016/S0261-2194(01)00103-X.
31. Rotenberg D, Krishna Kumar NK, Ullman DE, Montero-Astúa M, Willis DK, et al. (2009) Variation in Tomato spotted wilt virus titer in Frankliniella occidentalis and its association with frequency of transmission. Phytopathology 99: 404-410. doi:10.1094/PHYTO-99-4-0404. PubMed: 19271982.
32. Selman I, Brierley M, Pegg G, Hill T, (1961) Changes in the free amino acids and amides in tomato plants inoculated with tomato spotted wilt virus. Ann Appl Biol 49: 601-615. doi:10.1111/j.1744-7348.1961.tb03657.x.
33. Catoni M, Miozzi L, Fiorilli V, Lanfranco L, Accotto GP, (2009) Comparative analysis of expression profiles in shoots and roots of tomato systemically infected by Tomato spotted wilt virus reveals organ-specific transcriptional responses. Mol Plant Microbe Interact 22: 1504-1513. doi:10.1094/MPMI-22-12-1504. PubMed: 19888816.
34. Leon-Reyes A, Van der Does D, De Lange ES, Delker C, Wasternack C, et al. (2010) Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta 232: 1423-1432. doi:10.1007/s00425-010-1265-z. PubMed: 20839007.
35. Howe GA, Lee GI, Itoh A, Li L, DeRocher AE, (2000) Cytochrome P450-dependent metabolism of oxylipins in tomato. Cloning and expression of allene oxide synthase and fatty acid hydroperoxide lyase. Plant Physiol 123: 711-724. doi:10.1104/pp.123.2.711. PubMed: 10859201.
36. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, et al. (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147: 1358-1368. doi:10.1104/pp.108.121392. PubMed: 18539774.
37. Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC, (2004) Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiol 135: 483-495. doi:10.1104/pp.103.038315. PubMed: 15122016.
38. Li C, Williams MM, Loh Y-T, Lee GI, Howe GA, (2002) Resistance of cultivated tomato to cell content-feeding herbviores is regualted by the octadecanoid-signaling pathway. Plant Physiol 130: 494-503. doi:10.1104/pp.005314. PubMed: 12226528.
39. Koornneef A, Pieterse CMJ, (2008) Cross-talk in defense signaling. Plant Physiol 146: 839-844. doi:10.1104/pp.107.112029. PubMed: 18316638.
40. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, et al. (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97: 11655-11660. doi:10.1073/pnas.97.21.11655. PubMed: 11027363.
41. Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C, (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140: 249-262. PubMed: 16377744.
42. Sugio A, MacLean AM, Grieve VM, Hogenhout SA, (2011) Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proc Natl Acad Sci USA 108: E1254-E1263. doi:10.1073/pnas.1105664108. PubMed: 22065743.
43. Zhang T, Luan J-B, Qi J-F, Huang C-J, Li M, et al. (2012) Begomovirus-whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor. Mol Ecol 21: 1294-1304. doi:10.1111/j.1365-294X.2012.05457.x. PubMed: 22269032.
44. Lewsey MG, Murphy AM, MacLean D, Dalchau N, Westwood JH, et al. (2010) Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol Plant Microbe Interact 23: 835-845. doi:10.1094/MPMI-23-7-0835. PubMed: 20521947.
45. Conesa A, Götz S, (2008) Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int J Plants Genomics, 2008(2008): 619832. PubMed: 18483572.
46. Tabachnick BG, Fidell LS, (2001) Principal components and factor analysis. Using multivariate statistics. Boston: Allyn & Bacon. pp. pp. 582-652.
47. Rotenberg D, Thompson TS, German TL, Willis DK, (2006) Methods for effective real-time RT-PCR analysis of virus-induced gene silencing. J Virol Methods 138: 49-59. doi:10.1016/j.jviromet.2006.07.017. PubMed: 16959330.
48. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. doi:10.1093/nar/29.9.e45. PubMed: 11328886.
49. Whitfield AE, Kumar NKK, Rotenberg D, Ullman DE, Wyman EA, et al. (2008) A soluble form of the Tomato spotted wilt virus (TSWV) glycoprotein GN (GN-S) inhibits transmission of TSWV by Frankliniella occidentalis. Phytopathology 98: 45-50. doi:10.1094/PHYTO-98-1-0045. PubMed: 18943237.
50. Pan X, Welti R, Wang X, (2008) Simultaneous quantifictaion of major phytohormones and related compounds in crude plant extracts by liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69: 1773-1781. doi:10.1016/j.phytochem.2008.02.008. PubMed: 18367217.
51. El Fahaam YM, Fegla GI, Wagih EE, El-Karyoni HA, (1990) Biochemical changes in lettuce plants infected with lettuce mosaic virus. J Agric Sci 2: 271-277.
52. Broderick GA, Kang JH, (1980) Automated simultaneous determination of ammonia and total amino acids in ruminal fluid and in vitro media. J Dairy Sci 63: 64-75. doi:10.3168/jds.S0022-0302(80)82888-8. PubMed: 7372898.