Root and shoot jasmonic acid induced plants differently affect the performance of Bemisia tabaci and its parasitoid Encarsia formosa

Basic and Applied Ecology

Volumn 14, Issue 8, 2013, Pages 670-679

  Li, Shao Jian ^a   Xue, Xia ^a   Ren, Shun Xiang ^a   Cuthbertson, Andrew G S ^b   van Dam, Nicole M ^c   Qiu, Bao Li ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b FOOD AND ENVIRONMENT RESEARCH AGENCY   (United Kingdom)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

Bemisia tabaci; Encarsia formosa; Induced plant defense; Jasmonic acid; Phloem feeding insect; Tritrophic interactions

Indexed keywords

ALEYRODIDAE; APHELINIDAE; BEMISIA TABACI; BRASSICA OLERACEA; BRASSICA OLERACEA VAR. ALBOGLABRA; BRASSICA OLERACEA VAR. ITALICA; ENCARSIA FORMOSA; HEXAPODA;

EID: 84889570550     PISSN: 14391791     EISSN: 16180089     Source Type: Journal    
DOI: 10.1016/j.baae.2013.08.011     Document Type: Article

References (70)

1. Ahmed M.Z., De Barro P.J., Greeff J.M., Ren S.X., Naveed M., Qiu B.L. Genetic identity of the Bemisia tabaci species complex and association with high cotton leaf curl disease (CLCuD) incidence in Pakistan. Pest Management Science 2011, 67:307-317.
2. Baldwin I.T. Herbivory simulations in ecological research. Trends Ecology & Evolution 1990, 5:91-93.
3. Benrey B., Denno R.F. The slow-growth-high-mortality hypothesis: A test using the cabbage butterfly. Ecology 1997, 78:987-999.
4. Bodenhausen N., Reymond P. Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Molecular Plant Microbe Interactions 2007, 20:1406-1420.
5. Birch L.C. The intrinsic rate of natural increase in an insect population. Journal of Animal Ecology 1948, 17:15-26.
6. Brown J.K., Frohlich D.R., Rosell R.C. The sweetpotato or silverleaf whiteflies: Biotypes of Bemisia tabaci or a species complex?. Annual Review of Entomology 1995, 40:511-534.
7. Brown J.K., Czosnek H. Whitefly transmission of plant viruses. Advances in botanical research 2002, 65-100. Academic Press, New York, NY. R.T. Plumb, J.A. Callow (Eds.).
8. Bukovinszky T., van Veen F.J.F., Jongema Y., Dicke M. Direct and indirect effects of resource quality on food web structure. Science 2008, 319:804-807.
9. Byrne F.J., Castle S., Prabhaker N., Toscano N.C. Biochemical study of resistance to imidalcoprid in B biotype Bemisia tabaci from Guatemala. Pest Management Science 2003, 59:347-352.
10. Cipollini D.F., Sipe M.L. Jasmonic acid treatment and mammalian herbivory differentially affect chemical defenses and growth of wild mustard (Brassica kaber). Chemoecology 2001, 11:137-143.
11. Cock M.J.N. Bemisia tabaci - A literature survey on the cotton whitefly with an annotated bibliography 1986, 21. FAO/CAB International Institute of Biological Control, Ascot, UK.
12. Costa H.S., Brown J.K. Variation in biological characteristics and esterase patterns among populations of Bemisia tabaci, and the association of one population with silverleaf symptom induction. Entomologia Experimentalis et Applicata 1991, 61:211-219.
13. Costa H.S., Brown J.K., Sivasupramaniam S., Bird J. Regional distribution, insecticide resistance, and reciprocal crosses between the A-biotype and B-biotype of Bemisia tabaci. Insect Science and Its Application 1993, 14:255-266.
14. Cuthbertson A.G.S., Walters K.F.A. Pathogenicity of the entomopathogenic fungus Lecanicillium muscarium against the sweetpotato whitefly Bemisia tabaci under laboratory and glasshouse conditions. Mycopathologia 2005, 160:315-319.
15. Cuthbertson A.G.S., Buxton J.H., Blackburn L.F., Mathers J.J., Robinson K.A., Powell M.E., et al. Eradicating Bemisia tabaci Q biotype on poinsettia plants in the UK. Crop Protection 2012, 42:42-48.
16. Dalton R. Whitefly infestations - The Christmas invasion. Nature 2006, 443(7114):898-900.
17. De Barro P.J., Hart P.J. Mating interactions between two biotypes of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae) in Australia. Bulletin of Entomological Research 2000, 90(2):103-112.
18. De Barro P.J., Hart P.J., Morton R. The biology of two Eretmocerus spp. (Haldeman) and three Encarsia spp. Forster and their potential as biological control agents of Bemisia tabaci biotype B in Australia. Entomologia Experimentalis et Applicata 2000, 94(1):93-102.
19. De Barro P.J., Liu S.S., Boykin L.M., Dinsdale A.B. Bemisia tabaci: A statement of species status. Annual Review of Entomology 2011, 56:1-19.
20. Dicke M., de Boer J.G., Hofte M., Rocha-Granados M.C. Mixed blends of herbivore-induced plant volatiles and foraging success of carnivorous arthropods. Oikos 2003, 101(1):38-48.
21. Elbaz M., Halon E., Malka O., Malitsky S., Blum E., Aharoni A., et al. Asymmetric adaptation to indolic and aliphatic glucosinolates in the B and Q sibling species of Bemisia tabaci (Hemiptera: Aleyrodidae). Molecular Ecology 2012, 21:4533-4546.
22. Feng Y.T., Wu Q.J., Wang S.L., Chang X.L., Xie W., Xu B.Y., et al. Cross-resistance study and biochemical mechanisms of thiamethoxam resistance in B biotype Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science 2010, 66:313-318.
23. Gelman D.B., Blackburn M.B., Hu J.S. Identification of the molting hormone of the sweet potato (Bemisia tabaci) and greenhouse (Trialeurodes vaporariorum) whitefly. Journal of Insect Physiology 2005, 51:47-53.
24. Gerling D., Alomar O., Arno J. Biological control of Bemisia tabaci using predators and parasitoids. Crop Protection 2001, 20:779-799.
25. Harvey J.A. Factors affecting the evolution of development strategies in parasitoid wasps: The importance of functional constraints and incorporating complexity. Entomologia Experimentalis et Applicata 2005, 117:1-13.
26. Harvey J.A., van Dam N.M., Gols R. Interactions over four trophic levels: Foodplant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid. Journal of Animal Ecology 2003, 72:520-530.
27. He Y.X., Zhao J.W., Huang J., Weng Q.Y., Liang Z.S. Frequency distribution of residual acetylcholinesterase activity in presence of inhibitor and its relationship with insecticide resistance in different populations of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Acta Entomologica Sinica 2009, 52:1373-1378.
28. Hoddle M.S., van Driesche R.G., Sanderson J.P. Biology and use of the whitefly parasitoid Encarsia formosa. Annual Review of Entomology 1998, 43:645-669.
29. Ishaaya I. Pyriproxyfen, a novel insect growth regulator for controlling whiteflies: Mechanisms and resistance management. Pesticide Science 1995, 43:227-232.
30. Jansen J.J., Allwood J.M., Marsden-Edwards E., van der Putten W.H., Goodacre R., van Dam N.M. Metabolomic analysis of the interaction between plants and herbivores. Metabolomics 2009, 5:150-161.
31. Jiang N., Xu R., van Lenteren J.C., van Roermund H.J.W. Temporal and spatial analysis of greenhouse whitefly and its parasitoid Encarsia formosa in two types of greenhouse ecosystems. Journal of Applied Entomology 1999, 123(9):547-554.
32. Jones D.R. Plant viruses transmitted by whiteflies. European Journal of Plant Pathology 2003, 109:195-219.
33. Kessler A., Baldwin I.T. Plant responses to insect herbivory: The emerging molecular analysis. Annual Review of Plant Biology 2002, 53:299-328.
34. Koornneef A., Leon-Reyes A., Ritsema T., Verhage A., Den Otter F.C., van Loon L.C., et al. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiology 2008, 147:1358-1368.
35. Lawrence P.O. The biochemical and physiological effects of insect hosts on the development and ecology of their insect parasites - An overview. Archives of Insect Biochemistry and Physiology 1990, 13:217-228.
36. Liang Y.S., Choi Y.H., Kim H.K., Linthorst H.J.M., Verpoorte R. Metabolomic analysis of methyl jasmonate treated Brassica rapa leaves by 2-dimensional NMR spectroscopy. Phytochemistry 2006, 67:2503-2511.
37. Maia A., de H.Z., Luiz A.J.B., Campanhola C. Statistical inference on associated fertility life table parameters using jackknife technique: Computational aspects. Journal of Economic Entomology 2000, 93:511-518.
38. McConn M., Creelman R.A., Bell E., Mullet J.E., Browse J. Jasmonate is essential for insect defense Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:5473-5477.
39. Mithen R.F., Lewis B.G., Heaney R.K., Fenwick G.R. Glucosinolates of wild and cultivated Brassica species. Phytochemistry 1987, 26:1969-1973.
40. Moore J.P., Paul N.D., Whittaker J.B., Taylor J.E. Exogenous jasmonic acid mimics herbivore-induced systemic increase in cell wall bound peroxidase activity and reduction in leaf expansion. Function Ecology 2003, 17:549-554.
41. Ode P.J. Plant chemistry and natural enemy fitness: Effects on herbivore and natural enemy interactions. Annual Review of Entomology 2006, 51:163-185.
42. Oliveira M.R.V., Henneberry T.J., Anderson P. History, current status and collaborative research projects for Bemisia tabaci. Crop Protection 2001, 20:709-723.
43. Ozawa R., Arimura G., Takabayashi J., Shimoda T., Nishioka T. Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant and Cell Physiology 2000, 41:391-398.
44. Pang S.T., Wang L., Hou Y.H., Shi Z.H. Interspecific interference competition between Encarsia formosa and Encarsia sophia (Hymenoptera: Aphelinidae) in parasitizing Bemisia tabaci (Hemiptera: Aleyrodidae) on five tomato varieties. Insect Science 2011, 18(1):92-100.
45. Pierre P.S., Dugravot S., Cortesero A.M., Poinsot D., Raaijmakers C.E., Hassan H.M., et al. Broccoli and turnip plants display contrasting responses to belowground induction by Delia radicum infestation and phytohormone applications. Phytochemistry 2012, 73:42-50.
46. Poelman E.H., van Dam N.M., van Loon J.J.A., Vet L.E.M., Dicke M. Chemical diversity in Brassica oleracea affects biodiversity of insect herbivores. Ecology 2009, 90(7):1863-1877.
47. Polaszek A., Evans G.A., Bennet F.D. Encarsia parasitoids of Bemisia tabaci (Hymenoptera: Aphelinidae, Homoptera: Aleyrodidae): A preliminary guide to identification. Bulletin of Entomological Research 1992, 82:375-392.
48. Qiu B.L., De Barro P.J., He Y.R., Ren S.X. Suitability of Bemisia tabaci (Hemiptera: Aleyrodidae) instars for the parasitization by Encarsia bimaculata and Eretmocerus sp. nr. furuhashii (Hymenoptera: Aphelinidae) on glabrous and hirsute host plants. Biocontrol Science and Technology 2007, 17:823-839.
49. Qiu B.L., Coats S.A., Ren S.X., Idris A.M., Xu C.X., Brown J.K. Phylogenetic relationships of Bemisia tabaci (Homoptera: Aleyrodidae) populations from China and India, based on mtCOI DNA sequencing and host plants comparison. Progress in Natural Science 2007, 17:645-654.
50. Qiu B.L., Harvey J.A., Raaijmakers C.E., Vet L.E.M., van Dam N.M. Nonlinear effects of plant root and shoot jasmonic acid application on the performance of Pieris brassicae and its parasitoid Cotesia glomerata. Functional Ecology 2009, 23:496-505.
51. ® 9.2, User's Guide, Cary, NC 2008.
52. Soler R., Bezemer T.M., van der Putten W.H., Vet L.E.M., Harvey J.A. Root herbivore effects on above-ground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. Journal of Animal Ecology 2005, 74:1121-1130.
53. Soler R., Bezemer T.M., Cortesero A.M., van der Putten W.H., Vet L.E.M., Harvey J.A. Impact of foliar herbivory on the development of a root-feeding insect and its parasitoid. Oecologia 2007, 152:257-264.
54. Soler R., Badenes-Perez F.R., Broekgaarden C., Zheng S.J., David A., Boland W., et al. Plant-mediated facilitation between a leaf-feeding and a phloem-feeding insect in a brassicaceous plant: From insect performance to gene transcription. Functional Ecology 2012, 26(1):156-166.
55. Stansly P.A., Liu T.X. Selectivity of insecticides to Encarsia pergandiella (Hymenoptera: Aphelinidae), and endoparasitoid of Bemisia argentifolii (Hemiptera: Aleyrodidae). Bulletin of Entomological Research 1997, 87(5):525-531.
56. Tytgat T.O., Verhoeven K.J.F., Jansen J.J., Raaijmakers C.E., Bakx-Schotman T., McIntyre L.M., et al. Plants know where it hurts: Root and shoot jasmonic acid induction elicit differential responses in Brassica oleracea. PLoS ONE 2013, 8(6):e65502. 10.1371/journal.pone.0065502.
57. van Dam N.M., Harvey J.A., Wackers F.L., Bezemer T.M., van der Putten W.H., Vet L.E.M. Interactions between aboveground and belowground induced responses against phytophages. Basic and Applied Ecology 2003, 4:63-77.
58. van Dam N.M., Witjes L., Svatoš A. Interactions between aboveground and belowground induction of glucosinolates in two wild Brassica species. New Phytologist 2004, 161:801-810.
59. van Dam N.M., Raaijmakers C.E. Local and systemic induced responses to cabbage root fly larvae (Delia radicum) in Brassica nigra and B. oleracea. Chemoecology 2006, 16:17-24.
60. van Dam N.M., Oomen W.A.T. Root and shoot jasmonic acid applications differentially affect leaf chemistry and herbivore growth. Plant Signaling and Behavior 2008, 3:91-98.
61. van Dam N.M., Heil M. Multitrophic interactions below and above ground: En route to the next level. Journal of Ecology 2011, 99:77-88.
62. van Lenteren J.C., Drost Y.C., van Roermund H.J.W., Posthuma-Doodeman C.J.A.M. Aphelinid parasitoids as sustainable biological control agents in greenhouses. Journal of Applied Entomology 1997, 121:473-485.
63. van Nouhuys S., Laine A.L. Population dynamics and sex ratio of a parasitoid altered by fungal-infected diet of host butterfly. Proceedings of the Royal Society B - Biological Science 2008, 275:787-795.
64. Vet L.E.M. From chemical to population ecology: Infochemical use in an evolutionary context. Journal of Chemical Ecology 1999, 25:31-49.
65. Vet L.E.M., Dicke M. Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 1992, 37:141-172.
66. Vinson S.B., Iwantsch G.F. Host regulation by insect parasitoids. Quarterly Review of Biology 1980, 55:143-165.
67. Walling L.L. The myriad plant responses to herbivores. Journal of Plant Growth Regulation 2000, 19:195-216.
68. Wittstock U., Gershenzon J. Constitutive plant toxins and their role in defense against herbivores and pathogens. Current opinion in plant biology 2002, 5(4):300-307.
69. Yang N.W., Wan F.H. Host suitability of different instars of Bemisia tabaci biotype B for the parasitoid Eretmocerus hayati. Biological control 2011, 59(2):313-317.
70. Zarate S.I., Kempema L.A., Walling L.L. Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiology 2007, 143(2):866-875.