Molecular and chemical mechanisms involved in aphid resistance in cultivated tomato

New Phytologist

Volumn 187, Issue 4, 2010, Pages 1089-1101

  Digilio, Maria Cristina ^a   Corrado, Giandomenico ^a   Sasso, Raffaele ^a   Coppola, Valentina ^a   Iodice, Luigi ^a   Pasquariello, Marianna ^a   Bossi, Simone ^b   Maffei, Massimo E ^b   Coppola, Mariangela ^a   Pennacchio, Francesco ^a   Rao, Rosa ^a   Guerrieri, Emilio ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Aphid parasitoid; Aphidius ervi; Gene expression; Macrosiphum euphorbiae; Solanum lycopersicum; Volatile organic compounds

Indexed keywords

APHID; FITNESS; FRUIT; GAS CHROMATOGRAPHY; GENE EXPRESSION; HOST-PARASITOID INTERACTION; INTEGRATED APPROACH; MASS SPECTROMETRY; MOLECULAR ANALYSIS; PLANT DEFENSE; VOLATILE ORGANIC COMPOUND;

CAMPANIA [ITALY]; ITALY;

APHIDIDAE; APHIDIUS ERVI; LYCOPERSICON ESCULENTUM; MACROSIPHUM EUPHORBIAE; SOLANUM;

EID: 77955758020     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03314.x     Document Type: Article

References (65)

1. Adams P. Identification of essential oil components by gas chromatography:quadrupole mass spectroscopy 2001, Carol Stream, IL, USA, Allured Publications
2. Agrawal AA, Tuzun S, Bent E. Induced plant defenses against pathogens and herbivores. Biochemistry, ecology, and agriculture 1999, St Paul, MN, USA, APS Press
3. Andreakis N, Giordano I, Pentangelo A, Fogliano V, Graziani G, Monti LM, Rao R. DNA fingerprinting and quality traits of Corbarino cherry-like tomato landraces. Journal of Agricultural and Food Chemistry 2004, 52:3366-3371.
4. Birch LC. The intrinsic rate of natural increase of an insect population. Journal of Animal Ecology 1948, 17:15-26.
5. Birkett MA, Campbell CAM, Chamberlain K, Guerrieri E, Hick AJ, Martin JL, Matthes M, Napier JA, Pettersson J, Pickett JA. New roles for cis-jasmone as an insect semiochemical and in plant defence. Proceedings of the National Academy of Sciences, USA 2000, 97:9329-9334.
6. Blight MM, Pickett JA, Wadhams LJ, Woodcock C. Antennal perception of oilseed rape, Brassica napus (Brassicaceae), volatiles by the cabbage seed weevil Ceutorhynchus assimilis (Coleoptera, Curculionidae). Journal of Chemical Ecology 1995, 21:1649-1664.
7. Boyko EV, Smith CM, Thara VK, Bruno JM, Deng YP, Starkey SR, Klaahsen DL. Molecular basis of plant gene expression during aphid invasion: wheat Pto- and Pti-likeA sequences are involved in interactions between wheat and Russian wheat aphid (Homoptera: Aphididae). Journal of Economic Entomology 2006, 99:1430-1445.
8. Bruce TJ, Matthes MC, Chamberlain K, Woodcock CM, Mohib A, Webster B, Smart LE, Birkett MA, Pickett JA, Napier JA. cis-Jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids. Proceedings of the National Academy of Sciences, USA 2008, 105:4553-4558.
9. de Bruyne M, Baker TC. Odor detection in insects: volatile codes. Journal of Chemical Ecology 2008, 34:882-897.
10. Caramante M, Rao R, Monti LM, Corrado G. Discrimination of 'San Marzano' accessions: a comparison of minisatellite, CAPS and SSR markers in relation to morphological traits. Scientia Horticulturae 2009, 120:560-564.
11. Casteel C, Walling LL, Paine T. Behavior and biology of the tomato psyllid, Bactericerca cockerelli, in response to the Mi-1.2 gene. Entomologia Experimentalis et Applicata 2006, 121:67-72.
12. Chakravarthy S, Tuori RP, D'Ascenzo MD, Fobert PR, Despres C, Martin GB. The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell 2003, 15:3033-3050.
13. Colazza S, McElfresh JS, Millar JG. Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. Journal of Chemical Ecology 2004, 30:945-964.
14. Corrado G, Arciello S, Fanti P, Fiandra L, Garonna A, Digilio MC, Lorito M, Giordana B, Pennacchio F, Rao R. The Chitinase A from the baculovirus AcMNPV enhances resistance to both fungi and herbivorous pests in tobacco. Transgenic Research 2008, 17:557-571.
15. Corrado G, Delli Bovi P, Ciliento R, Gaudio L, Di Maro A, Aceto S, Lorito M, Rao R. Inducible expression of a Phytolacca heterotepala ribosome-inactivating protein leads to enhanced resistance against major fungal pathogens in tobacco. Phytopathology 2005, 95:206-215.
16. Corrado G, Sasso R, Pasquariello M, Iodice L, Carretta A, Cascone P, Ariati L, Digilio MC, Guerrieri E, Rao R. Systemin regulates both systemic and volatile signalling in tomato plants. Journal of Chemical Ecology 2007, 33:669-681.
17. Dicke M. Behavioural and community ecology of plants that cry for help. Plant, Cell & Environment 2009, 32:654-665.
18. Du YJ, Poppy GM, Powell W. Relative importance of semiochemicals from first and second trophic level in host foraging behaviour of Aphidius ervi. Journal of Chemical Ecology 1996, 22:1591-1606.
19. Fazio G, Stevens MR, Scott JW. Identification of RAPD markers linked to fusarium crown and root rot resistance (Frl) in tomato. Euphytica 1999, 105:205-210.
20. Fidantsef AL, Stout MJ, Thaler JS, Duffey SS. Signal interactions in pathogen and insect attack: expression of lipoxygenase, proteinase inhibitor II, and pathogenesis-related protein P4 in the tomato, Lycopersicon esculentum. Physiological and Molecular Plant Pathology 1999, 54:97-114.
21. Fraser AM, Mechaber WL, Hildebrand JG. Electroantennographic and behavioral responses of the sphinx moth Manduca sexta to host plant headspace volatiles. Journal of Chemical Ecology 2003, 29:1813-1833.
22. Gatehouse JA. Plant resistance towards insect herbivores: a dynamic interaction. New Phytologist 2002, 156:145-169.
23. Giordano I, Pentangelo A, Villari G, Fasanaro G, Castaldo D. Caratteristiche agronomiche e idoneità alla trasformazione di pomodori dell'ecotipo "Corbarino" Industria Conserve 2000, 75:317-329. (In Italian with English abstract)
24. Girling RD, Madison R, Hassall M, Poppy GM, Turner JG. Investigations into plant biochemical wound-response pathways involved in the production of aphid-induced plant volatiles. Journal of Experimental Botany 2008, 59:3077-3085.
25. Glinwood R, Gradin T, Karpinska B, Ahmed E, Jonsson L, Ninkovic V. Aphid acceptance of barley exposed to volatile phytochemicals differs between plants exposed in daylight and darkness. Plant Signalling & Behavior 2007, 2:321-326.
26. Goggin FL, Williamson VM, Ullman DE. Variability in the response of Macrosiphum euphorbiae and Myzus persicae (Hemiptera: Aphididae) to the tomato resistance gene Mi. Environmental Entomology 2001, 30:101-106.
27. Guerrieri E, Digilio MC. Aphid-plant interactions: a review. Journal of Plant Interactions 2008, 3:223-232.
28. Guerrieri E, Pennacchio F, Tremblay E. Flight behaviour of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae) in response to plant and host volatiles. European Journal of Entomology 1993, 90:415-421.
29. Guerrieri E, Poppy GM, Powell W, Rao R, Pennacchio F. Plant to plant communication mediating in-flight orientation of Aphidius ervi. Journal of Chemical Ecology 2002, 28:1703-1715.
30. Hebert SL, Jia L, Goggin FL. Quantitative differences in aphid virulence and foliar symptom development on tomato plants carrying the Mi resistance gene. Environmental Entomology 2007, 36:458-467.
31. Howe GA, Jander G. Plant immunity to insect herbivores. Annual Review of Plant Biology 2008, 59:41-66.
32. James DG. Further field evaluation of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. Journal of Chemical Ecology 2005, 31:481-495.
33. James DG, Grasswitz TR. Synthetic herbivore-induced plant volatiles increase field captures of parasitic wasps. BioControl 2005, 50:871-880.
34. Kaloshian I, Kinsey MG, Ullman DE, Williamson VM. The impact of Meu 1-mediated resistance in tomato on longevity, fecundity and behavior of the potato aphid Macrosiphum euphorbiae. Entomologia Experimentalis et Applicata 1997, 83:181-187.
35. Kennedy GG. Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon. Annual Review of Entomology 2003, 48:51-72.
36. Lange WH, Bronson L. Insect pests of tomato. Annual Review of Entomology 1981, 26:345-371.
37. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 2001, 25:402-408.
38. Martin GB, Williams JGK, Tanksley SD. Rapid identification of markers linked to a Pseudomonas resistance gene in tomato by using random primers and near-isogenic lines. Proceedings of the National Academy of Sciences, USA 1991, 88:2336-2340.
39. Mysore KS, D'Ascenzo MD, He XH, Martin GB. Overexpression of the disease resistance gene Pto in tomato induces gene expression changes similar to immune responses in human and fruitfly. Plant Physiology 2003, 132:1901-1912.
40. Nicot N, Hausman JF, Hoffmann L, Evers D. Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. Journal of Experimental Botany 2005, 56:2907-2914.
41. Nombela G, Williamson VM, Muniz M. The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Molecular Plant-Microbe Interaction 2003, 16:645-649.
42. Park SJ, Huang YH, Ayoubi P. Identification of expression profiles of sorghum genes in response to greenbug phloem-feeding using cDNA subtraction and microarray analysis. Planta 2006, 223:932-947.
43. Poelman EH, van Loon JJA, Dicke M. Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends in Plant Science 2008, 13:534-541.
44. Qubbaj T, Reineke A, Zebitz CPW. Molecular interactions between rosy apple aphids, Dysaphis plantaginea, and resistant and susceptible cultivars of its primary host Malus domestica. Entomologia Experimentalis et Applicata 2005, 115:145-152.
45. Rao R, Corrado G, Bianchi M, Di Mauro A. (GATA)(4) DNA fingerprinting identifies morphologically characterized 'San Marzano' tomato plants. Plant Breeding 2006, 125:173-176.
46. Rassman S, Köllner TG, Degenhard J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 2005, 434:732-737.
47. Rohlf FJ, Sokal RR. Statistical tables 1995, 3rd edn, New York, NY, USA, WH Freeman and Co
48. Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the National Academy of Sciences, USA 1998, 95:9750-9754.
49. Ruiz JJ, Garcia-Martinez S, Pico B, Gao MQ, Quiros CF. Genetic variability and relationship of closely related Spanish traditional cultivars of tomato as detected by SRAP and SSR markers. Journal of the American Society for Horticultural Science 2005, 130:88-94.
50. Sasso R, Iodice L, Digilio MC, Carretta A, Ariati L, Guerrieri E. Host-locating response by the aphid parasitoid Aphidius ervi to tomato plant volatiles. Journal of Plant Interactions 2007, 2:175-183.
51. Sasso R, Iodice L, Pickett JA, Woodcock CM, Guerrieri E. Behavioural and electrophysiological responses of Aphidius ervi (Hymenoptera: Braconidae) to tomato plant volatiles. Chemoecology 2009, 19:195-201.
52. Singh DP, Singh A. Disease and insect resistance in plants 2005, Enfield, NH, USA, Science Publisher
53. Smith CM, Boyko EV. The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomologia Experimentalis et Applicata 2007, 122:1-16.
54. Sobir TO, Ohmori T, Murata M, Motoyoshi F. Molecular characterization of the SCAR markers tightly linked to the Tm-2 locus of the genus Lycopersicon. Theoretical and Applied Genetics 2000, 101:64-69.
55. Sokal RR, Rohlf FJ. Biometry 1981, 2nd edn, New York, NY, USA, WH Freeman and Co
56. Thompson GA, Goggin FL. Transcriptomics and functional genomics of plant defence induced by phloem-feeding insects. Journal of Experimental Botany 2006, 57:747-754.
57. Van der Meijden E, Klinkhamer PGI. Conflicting interests of plants and the natural enemies of herbivores. Oikos 2000, 89:202-208.
58. Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, Castañera P, Sanchez-Serrano JJ. Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proceedings of the National Academy of Sciences, USA 2001, 98:8139-8144.
59. Visser JH. Host odour perception in phytophagous insects. Annual Review of Entomology 1986, 31:121-144.
60. Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, Hogers R, Frijters A, Groeendijk J, Diergaarde P, Reijans M. The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nature Biotechnology 1998, 16:1365-1369.
61. Vosman B, Arens P, Ruskortekaas W, Smulders MJM. Identification of highly polymorphic DNA regions in tomato. Theoretical and Applied Genetics 1992, 85:239-244.
62. Wäckers FL, Bonifay C. How to be sweet? Extrafloral nectar allocation by Gossypium hirsutum fits optimal defense theory predictions. Ecology 2004, 85:1512-1518.
63. Walgenbrach JF. Effect of potato aphid (Homoptera: Aphididae) on yield, quality, and economics of staked-tomato production. Journal of Economic Entomology 1997, 90:996-1004.
64. Williamson VM, Ho JY, Wu FF, Miller N, Kaloshian I. A PCR-based marker tightly linked to the nematode resistance gene, Mi, in tomato. Theoretical and Applied Genetics 1994, 87:757-763.
65. Zangerl AR. Evolution of induced plant responses to herbivores. Basic and Applied Ecology 2003, 4:91-103.