Reduction in the fitness of bemisia tabaci fed on three previously infested tomato genotypes differing in the jasmonic acid pathway

Environmental Entomology

Volumn 41, Issue 6, 2012, Pages 1443-1453

  Cui, Hongying ^a,b   Sun, Yucheng ^a   Su, Jianwei ^a   Li, Chuanyou ^c   Ge, Feng ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b YANGTZE UNIVERSITY   (China)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

Bemisia tabaci; jasmonic acid; salicylic acid; tomato; whitefly preconditioning

Indexed keywords

AMINO ACID; CYCLOPENTANE DERIVATIVE; JASMONIC ACID; OXYLIPIN; PHENOL DERIVATIVE; PROANTHOCYANIDIN; SALICYLIC ACID;

AMINO ACID; BIOTYPE; EGG; FECUNDITY; FITNESS; FRUIT; GENOTYPE; LARVA; SALICYLIC ACID; SUGAR; TANNIN; WHITEFLY;

ANIMAL; ARTICLE; CARBOHYDRATE METABOLISM; EGG LAYING; FERTILITY; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; HEMIPTERA; HERBIVORY; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; TOMATO;

AMINO ACIDS; ANIMALS; CARBOHYDRATE METABOLISM; CYCLOPENTANES; FERTILITY; GENOTYPE; HEMIPTERA; HERBIVORY; LYCOPERSICON ESCULENTUM; OVIPOSITION; OXYLIPINS; PHENOLS; PROANTHOCYANIDINS; SALICYLIC ACID; SIGNAL TRANSDUCTION;

ALEYRODIDAE; BEMISIA TABACI; LYCOPERSICON ESCULENTUM;

EID: 84871533803     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/EN11264     Document Type: Article

References (63)

1. Bi, J. L., G. R. Ballmer, D. L. Hendrix, T. J. Henneberry, and N. C. Toscano. 2001. Effect of cotton nitrogen fertilization on Bemisia argentifolii populations and honeydew production. Entomol. Exp. Appl. 99: 25-36.
2. Bi, J. L., N. C. Toscano, and M. A. Madore. 2003. Effects of urea fertilizer application on soluble protein and free amino acids content of cotton petioles in relation to silver leaf whitefly (Bemisia argentifolii) populations. J. Chem. Ecol. 29: 747-761.
3. Bird, T. L., and K. Krü ger. 2006. Response of the polyphagous whitefly Bemisia tabaci B-biotype (Hemiptera: Aleyrodidae) to crop diversification-influence of multiple sensory stimuli on activity and fecundity. Bull. Entomol. Res. 96: 15-23.
4. Blackmer, J. L., and D. N. Byrne. 1999. Changes in amino acids in Cucumis melo in relation to life-history traits and flight propensity of Bemisia tabaci. Entomol. Exp. Appl. 93: 29-40.
5. Buell, C. R. 1998. Arabidopsis: a weed leading the field of plant-pathogen interactions. Plant Physiol. Biochem. 36: 177-186.
6. Chen, F. J., G. Wu, and F. Ge. 2004a. Growth, development and reproduction of the cotton bollworm Helicoverpa armigera (Hü bner) reared on milky grains of wheat grown in elevated CO2 concentration. Chin. Acta Entomol. Sin. 47: 774-779.
7. Chen, J., H. J. McAuslane, R. B. Carle, and S. E.Webb. 2004b. Impact of Bemisia argentifolii (Homoptera: Auchenorrhyncha: Aleyrodidae) infestation and squash silverleaf disorder on zucchini yield and quality. J. Econ. Entomol. 97: 2083-2094.
8. Chi, H. 1988. Life-table analysis incorporating both sexes and variable development rate among individuals. Environ. Entomol. 17: 26-34.
9. Chi, H. 2004. TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. (http://140.120. 197.173/Ecology/Download/Twosex- MSChart.zip).
10. Chi, H., and H. Liu. 1985. Two new methods for the study of insect population ecology. Bull. Inst. Zool. Acad. Sin. 24: 225-240.
11. Cooper, W. R., L. Jia, and F. L. Goggin. 2004. Acquired and R-genemediated resistance against the potato aphid in tomato. J. Chem. Ecol. 30: 2527-2542.
12. De Vos, M., V. R. Van Oosten, R.M.P. Van Poecke, J. A. Van Pelt, M. J. Pozo, M. J. Mueller, A. J. Buchala, L. C. Van Loon, M. Dicke, and C.M.J. Pieterse. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant-Microbe Interact. 18: 923-937.
13. Denno, R. F., and G. K. Roderick. 1992. Density-related dispersal in planthoppers: effects of interspecific crowding. Ecology 73: 1323-1334.
14. Denno, R. F., M. S. McClure, and J. R. Ott. 1995. Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu. Rev. Entomol. 40: 297-331.
15. Gennadius, P. 1889. Disease of tobacco plantations in Trikonia: the aleurodid of tobacco. Ellenike Georgia 5: 1-3.
16. Goggin, F. L., V. M. Williamson, and D. E. Ullman. 2001. Variability in the response of Macrosiphum euphorbiae and Myzus persicae (Hemiptera: Aphididae) to the tomato resistance gene Mi. Environ. Entomol. 30: 101-106.
17. Heidel, A. J., and I. T. Baldwin. 2004. Microarray analysis of salicylic acid and jasmonic acid-signalling in responses of Nicotiana attenuate to attack by insects from multiple feeding guilds. Plant Cell Environ. 27: 1362-1373.
18. Hunter, M. D., and P. W. Price. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73: 724-732.
19. Inbar, M., A. Eshel, and D. Wool. 1995. Interspecific competition among phloem-feeding insects mediated by induced host-plant sinks. Ecology 76: 1506-1515.
20. Inbar, M., H. Doostdar, G. L. Leibee, and R. T. Mayer. 1999. The role of plant rapidly induced responses in asymmetric interspecific interactions among insect herbivores. J. Chem. Ecol. 25: 1961-1979.
21. Irigoyen, J. J., D. W. Emerich, and M. Sanchez-Dlaz. 1992. Water stress induced changes in concentrations of proline and total soluble sugar in nodulated alfalfa (Medicago sativa) plants. Physiol. Plant 84: 67-72.
22. Jiu, M., X. P. Zhou, L. Tong, J. Xu, X. Yang, F. H. Wan, and S. S. Liu. 2007. Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS ONE 2: e182. doi: 10.1371/journal.pone.0000182.
23. Joern, A., and S. T. Behmer. 1997. Importance of dietary nitrogen and carbohydrates to survival, growth, and reproduction in adults of the grasshopper Ageneotettix deorum (Orthoptera: Acrididae). Oecologia 112: 201-208.
24. Jormalainen, V., T. Honkanen, and N. Heikkila. 2001. Feeding preferences and performance of a marine isopod on seaweed hosts-cost of habitat selection. Mar. Ecol. Prog. Ser. 220: 219-230.
25. Kainulainen, P., J. Holopainen, and T. Holopainen. 2000. Combined effects of ozone and nitrogen on secondary compounds, amino acids, and aphid performance in Scots pine seedlings. J. Environ. Qual. 29: 334-342.
26. Karban, R., and I. T. Baldwin. 1997. Induced responses to herbivory. University of Chicago Press, Urbana-Champaign, IL.
27. Kempema, L. A., X. P. Cui, F. M. Holzer, and L. L. Walling. 2007. Arabidopsis Transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. similarities and distinctions in responses to aphids. Plant Physiol. 143: 849-865.
28. Kessler, A., and I. T. Baldwin. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291: 2141-2144.
29. Kujala, T. S., J. M. LoPonen, K. D. Klika, and K. Pihlaja. 2000. Phenolics and betacyanins in red beet root (Beta vulgaris) root: distribution and effect of cold storage on the content of total phenolics and three individual compounds. J. Agric. Food Chem. 48: 5338-5342.
30. Kusnierczyk, A., P. Winge, T. S. Jorstad, J. Troczynska, J. T. Rossiter, and A. M. Bones. 2008. Towards global understanding of plant defence against aphids-timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant Cell Environ. 31: 1097-1115.
31. Larson, K. C., and T. G. Whitham. 1991. Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia 88: 15-21.
32. Li, C., G. Liu, C. Xu, G. Lee, P. Bauer, M. Ganal, H. Ling, and G. A. Howe. 2003. The tomato suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemicwoundsignal for defense gene expression. Plant Cell 15: 1646-1661.
33. Li, Q., Q. G. Xie, J. Smith-Becker, D. A. Navarre, and I. Kaloshian. 2006. Mi-1-mediated aphid resistance involves salicylic acid andmitogen-activated protein kinase signaling cascades. Mol. Plant-Microbe Interact. 19: 655-664.
34. Mansour, M. H., N. M. Zohdy, S. E. El-Gengaihi, and A. E. Amr. 1997. The relationship between tannins concentration in some cotton varieties and susceptibility to piercing sucking insects. J. Appl. Entomol. 121: 321-325.
35. Mauricio, R., M. D. Rausher, and D. S. Burdick. 1997. Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78: 1301-1311.
36. Mayer, R. T., M. Inbar, C. L. McKenzie, R. Shatters, V. Borowicz, U. Albrecht, C. A. Powell, and H. Doostdar. 2002. Multitrophic interactions of the silverleaf whitefly, host plants, competing herbivores, and phytopathogens. Arch. Insect Biochem. Physiol. 51: 151-69.
37. McGurl, B., G. Pearce, M. Orozco-Cardenas, and C. A. Ryan. 1992. Structure, expression, and antisense inhibition of the systemin precursor gene. Science 255: 1570-1573.
38. McGurl, B., M. Orozco-Cardenas, G. Pearce, and C. A. Ryan. 1994. Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. Proc. Natl. Acad. Sci. U.S.A. 91: 9799-9802.
39. Messina, F. J., R. Taylor, and M. E. Karren. 2002. Divergent responses of two cereal aphids to previous infestation of their host plant. Entomol. Exp. Appl. 16: 43-50.
40. Murugan, M., and N. Dhandapani. 2007. Induced systemic resistance activates defense responses to interspecific insect infestations on tomato. J. Vegetable Sci. 28: 43-62.
41. Nombela, G., E. Garzo, M. Duque, and M. Muniz. 2009. Preinfestations of tomato plants by whiteflies (Bemisia tabaci) or aphids (Macrosiphum euphorbiae) induce variable resistance or susceptibility responses. Bull. Entomol. Res. 99: 183-191.
42. Ohgushi, T. 2005. Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu. Rev. Ecol. Evol. Syst. 36: 81-105.
43. Pegadaraju, V., C. Knepper, J. Reese, and J. Shah. 2005. Premature leaf senescence modulated by the Arabidopsis Phytoalexin Deficient4 gene is associated with defence against the phloem-feeding green peach aphid. Plant Physiol. 139: 1927-1934.
44. Petersen, M. K., and J. P. Sandström. 2001. Outcome of indirect competition between two aphid species mediated by responses in their common host plant. Funct. Ecol. 15: 525-534.
45. Poelman, E. H., C. Broekgaarden, J.J.A. Van Loon, and M. Dicke. 2008. Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol. Ecol. 17: 3352-3365.
46. Ren, Q., L. Z. Cao, J. W. Su, M. H. Xie, Q. W. Zhang, and X. X. Li. 2010. Volatile emissions from the invasive weed Eupatorium adenophorum induced by Aphis gossypii feeding and methyl jasmonate treatment. Weed Sci. 58: 252-257.
47. Rodriguez-Saona, C., J. A. Chalmers, S. Raj, and J. S. Thaler. 2005. Induced plant responses to multiple damagers: differential effects of an herbivore and its parasitoid. Oecologia 143: 566-577.
48. Sanchez-Hernandez, C., M. G. Lopez, and J. P. Delano-Frier. 2006. Reduced levels of volatile emissions in jasmonatedeficient spr2 tomato mutants favour oviposition by insect herbivores. Plant Cell Environ. 29: 546-557.
49. Sandström, J., and J. Pettersson. 1994. Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. J. Insect Physiol. 40: 947-955.
50. Simpson, S. J., J. D. Abisgold, and A. E. Douglas. 1995. Response of the pea aphid (Acrythosiphon pisum) to variation in dietary levels of sugar and amino acids: the significance of amino acid quality. J. Insect Physiol. 41: 71-75.
51. Sokal, R. R., and F. J. Rohlf. 1995. Biometry, 3rd ed. W.H. Freeman, San Francisco, CA.
52. Strong, D. R., J. H. Lawton, and R. Southwood. 1984. Insects on plants. Community patterns and mechanisms. Blackwell Scientific, Oxford. England.
53. Sun, Y. C., J. Yin, H. F. Cao, C. Y. Li, L. Kang, and F. Ge. 2011. Elevated CO2 influences nematode-induced defense responses of tomato genotypes differing in the JA pathway. PLoS ONE 6: e19751.
54. Terrill, T. H., A. M. Rowan, G. B. Douglas, and T. N. Barry. 1992. Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentrates meals and cereal grains. J. Sci. Food Agric. 58: 321-329.
55. Truman, W. M., M. H. Bennett, C.G.N. Turnbull, and M. R. Grant. 2010. Arabidopsis Auxin mutants are compromised in systemic acquired resistance and exhibit eberrant accumulation of various indolic compounds. Plant Physiol. 152: 1562-1573.
56. Walling, L. L. 2000. The myriad plant responses to herbivores. J. Plant Growth Regul. 19: 195-216.
57. Walling, L. L. 2008. Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol. 146: 859-866.
58. Weibull, J. 1987. Season changes in the free amino acids of oat and barley phloem sap in relation to lant growth stage and growth of Rhopalosiphum padi. Ann. Appl. Biol. 111: 729-737.
59. Wei, J. N., L. H. Wang, J. H. Zhao, C. Y. Li, F. Ge, and L. Kang. 2011. Ecological trade-offs between jasmonic acid-dependent direct and indirect plant defences in tritrophic interactions. New Phytol. 189: 557-567.
60. Williams, K. S., and J. H. Myers. 1984. Previous herbivore attack of red alder may improve food quality for fall webworm larvae. Oecologia 63: 166-170.
61. Wu, J. Q., and I. T. Baldwin. 2009. Herbivory-induced signalling in plants: perception and action. Plant Cell Environ. 32: 1161-1174.
62. Yin, J., Y. C. Sun, G. Wu, M. N. Parajulee, and F. Ge. 2009. Noeffects of elevatedCO2 on the population relationship between cotton bollworm, Helicoverpa armigera Hubner (Lepidoptera: Noctuidae), and its parasitoid, Microplitis mediator Haliday (Hymenoptera: Braconidae). Agric. Ecosyst. Environ. 132: 267-275.
63. Zarate, S. I., L. A. Kempema, and L. L. Walling. 2007. Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol. 143: 866-875.