The Behavioral Response of Nilaparvata Lugens to Rice Volatiles Induced by Chilo Suppressalis

doi:10.16409/j.cnki.2095-039x.2022.11.012

Abstract

Abstract: Previous studies showed that the brown planthoppers (BPH), Nilaparvata lugens, exhibited a strong preference to rice plants that had been infested by the rice striped stem borer (SSB), Chilo suppressalis. In order to identify the rice volatiles that affect the host-searching behavior of BPH, we tested the responses of BPH to 15 key rice volatile compounds induced by SSB infestation using H-tube olfactometer. The results showed that the four compounds including β-caryophyllene, 2-nonanone, germacrene D and (3E)-4,8-dimethyl-1,3,7-nonatriene were significantly attractive to BPH compared to the control (hexane). In contrast, the three compounds including methyl salicylate, 2-undecanone, and (3E,7E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene exhibited significant repellence to BPH. No effect on BPH behaviors were detected in 8 compounds, α-pinene, 2-tridecanone, (E)-2-heptenyl acetate, tridecanal, benzyl benzoate, isophorone, 2-pentadecanone, o-cymene, and isopropyl myristate. In summary, rice plants infested by SSB caterpillar release volatiles both attractive and repellent to BPH, and the preference of BPH to SSB-infested rice plants is caused by combined effects of multiple volatile compounds emitted by SSB-infested plants. These results provide a basis for the preparation of repellents or attractants for controlling the brown planthoppers.

Key words: Chilo suppressalis, Nilaparvata lugens, herbivore-induced rice volatiles, attraction, repellence

CLC Number:

S476

WANG Xiaolong, SU Shuangli, HU Xiaoyun, YIN Xinming, LI Yunhe. The Behavioral Response of Nilaparvata Lugens to Rice Volatiles Induced by Chilo Suppressalis[J]. Chinese Journal of Biological Control, 2023, 39(4): 970-977.

References

[1] Heil M. Herbivore-induced plant volatiles:targets, perception and unanswered questions[J]. New Phytologist, 2014, 204(2):297-306.
[2] Poelman E H. From induced resistance to defence in plant-insect interactions[J]. Entomologia Experimentalis et Applicata, 2015, 157(1):11-17.
[3] Poelman E H, Dicke M. Plant-mediated interactions among insects within a community ecological perspective[J]. Annual Plant Reviews, 2014, 47:309-337.
[4] Turlings T C J, Erb M. Tritrophic interactions mediated by herbivore-induced plant volatiles:mechanisms, ecological relevance, and application potential[J]. Annual Review of Entomology, 2018, 63(1):433-452.
[5] Zhu F, Broekgaarden C, Weldegergis B T, et al. Parasitism overrides herbivore identity allowing hyperparasitoids to locate their parasitoid host using herbivore-induced plant volatiles[J]. Molecular Ecology, 2015, 24(11):2886-2899.
[6] Dicke M, Baldwin I T. The evolutionary context for herbivore-induced plant volatiles:beyond the 'cry for help'[J]. Trends in Plant Science, 2010, 15(3):167-175.
[7] He J, Fandino R A, Halitschke R, et al. An unbiased approach elucidates variation in (S)-(+)-linalool, a context-specific mediator of a tri-trophic interaction in wild tobacco[J]. Proceedings of the National Academy of Sciences, 2019, 116(29):14651-14660.
[8] Erb M. Plant defenses against herbivory:closing the fitness gap[J]. Trends in Plant Science, 2017, 23(3):187-194.
[9] Fatouros N E, Dicke M, Mumm R, et al. Foraging behavior of egg parasitoids exploiting chemical information[J]. Behavioral Ecology, 2008, 19(3):677-689.
[10] Dicke M, Van Loon J J A, Soler R. Chemical complexity of volatiles from plants induced by multiple attack[J]. Nature Chemical Biology, 2009, 5(5):317-324.
[11] 娄永根, 程家安. 虫害诱导的植物挥发物:基本特性、生态学功能及释放机[J]. 生态学报, 2000, 20(6):1097-1106.
[12] Kessler A, Baldwin I T. Defensive function of herbivore-induced plant volatile emissions in nature[J]. Science, 2001, 291(5511):2141-2144.
[13] Jiao Y, Hu X, Peng Y, et al. Bt rice plants may protect neighbouring non-Bt rice plants against the striped stem borer, Chilo suppressalis[J]. Proceedings of the Royal Society B-Biological Sciences, 2018, 285(1883):20181283.
[14] Sun X L, Wang G C, GAO Y. Volatiles emitted from tea plants infested by Ectropis obliqua larvae are attractive to conspecific moths[J]. Journal of Chemical Ecology, 2014, 40(10):1080-1089.
[15] Carroll M J, Schmelz E A, Meagher R L, et al. Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings[J]. Journal of Chemical Ecology, 2006, 32(9):1911-1924.
[16] Schuman M C, Baldwin I T, et al. Field studies reveal functions of chemical mediators in plant interactions[J]. Chemical Society Reviews, 2018, 47(14):5338-5353.
[17] Joo Y, Schuman M C, Goldberg J K, et al. Herbivore-induced volatile blends with both "fast" and "slow" components provide robust indirect defence in nature[J]. Functional Ecology, 2018, 32(1):136-149.
[18] Bernasconi M L, Turlings T C J, Ambrosetti L, et al. Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis[J]. Entomologia Experimentalis et Applicata, 1998, 87(2):133-142.
[19] Delphia C M, Mescher M C, De Moraes C M. Induction of plant volatiles by herbivores with different feeding habits and the effects of induced defenses on host-plant selection by thrips[J]. Journal of Chemical Ecology, 2007, 33(5):997-1012.
[20] Bolter C J, Dicke M, Loon J J A V, et al. Attraction of colorado potato beetle to herbivore-damaged plants during herbivory and after its termination[J]. Journal of Chemical Ecology, 1997, 23(4):1003-1023.
[21] Kugimiya S, Shimoda T, Tabata J, et al. Present or past herbivory:a screening of volatiles released from Brassica rapa under caterpillar attacks as attractants for the solitary parasitoid, Cotesia vestali[J]. Journal of Chemical Ecology, 2010, 36(6):620-628.
[22] Qiao H, Lu P, Liu S, et al. Volatiles from Aquilaria sinensis damaged by Heortia vitessoides larvae deter the conspecific gravid adults and attract its predator Cantheconidea concinna[J]. Scientific Reports, 2018, 8(1):1-15.
[23] 周强, 徐涛, 张古忍. 虫害诱导的水稻挥发物对褐飞虱的驱避作用[J]. 昆虫学报, 2003, 46(6):739-744.
[24] Liu S, Zhao J, Hamada C, et al. Identification of attractants from plant essential oils for Cyrtorhinus lividipennis, an important predator of rice planthoppers[J]. Journal of Pest Science, 2019, 92(2):769-780.
[25] Wang X, Liu Q, Meissle M, et al. Bt rice could provide ecological resistance against nontarget planthoppers[J]. Plant Biotechnol Journal, 2018, 16(10):1748-1755.
[26] Hu X, Su S, Liu Q, et al. Caterpillar-induced rice volatiles provide enemy-free space for the offspring of the brown planthopper[J]. eLife, 2020, 9:e55421.
[27] Khan Z R, Saxena R C. Effect of steam distillate extracts of resistant and susceptible rice cultivars on behavior of Sogatella furcifera (Homoptera:Delphacidae)[J]. Journal of Economic Entomology, 1986, 79(4):928-935.
[28] 刘芳, 娄永根, 程家安. 稻株挥发物在调节褐飞虱、白背飞虱种内种间关系中的作用[J]. 中国水稻科学, 2002, 16(2):162-166.
[29] Erb M, Meldau S, Howe G A. Role of phytohormones in insect-specific plant reactions[J]. Trends in Plant Science, 2012, 17(5):250.
[30] Signoretti A G C, Peñaflor M, Bento J M S. Fall armyworm, Spodoptera frugiperda (JE Smith) (Lepidoptera:Noctuidae), female moths respond to herbivore-induced corn volatiles[J]. Neotropical entomology, 2012, 41(1):22-26.
[31] 张祯海. 水稻种植技术及病虫害防治技术[J]. 中国农业信息, 2016(17):108.
[32] 李威, 林拥军, 周菲. 萜烯同系物DMNT和TMTT的研究进展[J]. 植物保护学报, 2018, 45(5):25-32.
[33] Xiao Y, Wang Q, Erb M, et al. Specific herbivore-induced volatiles defend plants and determine insect community composition in the field[J]. Ecology Letters, 2012, 15(10):1130-1139.
[34] Fujii T, Hori M, Matsuda K. Attractants for rice leaf bug, Trigonotylus caelestialium (Kirkaldy), are emitted from flowering rice panicles[J]. Journal of Chemical Ecology, 2010, 36(9):999-1005.
[35] Wang Q, Xin Z J, Li J, et al. (E)-β-caryophyllene functions as a host location signal for the rice white-backed planthopper Sogatella furcifera[J]. Physiological and Molecular Plant Pathology, 2015, 91:106-112.
[36] Robert C A M, Erb M, Duployer M. Herbivore-induced plant volatiles mediate host selection by a root herbivore[J]. The New Phytologist, 2012, 194(4):1061-1069.
[37] Rasmann S, Köllner T G, Degenhardt J, et al. Recruitment of entomopathogenic nematodes by insect-damaged maize roots[J]. Nature, 2005, 434(7034):732-737.
[38] Mozuraitis R, Stranden M, Ramirez M I, et al. (-)-Germacrene D increases attraction and oviposition by the tobacco budworm moth Heliothis virescens[J]. Chemical Senses London, 2002, 27(6):505-509.
[39] Dicke M, Van Beek T A, Posthumus M A, et al. Isolation and identification of volatile kairomone that affects acarine predatorprey interactions:involvement of host plant in its production[J]. Journal of Chemical Ecology, 1990, 16(2):381-396.
[40] Turlings T C J, Scheepmaker J W A, Vet L E M, et al. How contact foraging experiences affect preferences for host-related odors in the larval parasitoid Cotesia marginiventris (Cresson) (Hymenoptera:Braconidae)[J]. Journal of Chemical Ecology, 1990, 16(5):1577-1589.
[41] Arimura G I, Ozawa R, Shimoda T, et al. Herbivory-induced volatiles elicit defence genes in lima bean leaves[J]. Nature, 2000, 406(6795):512-515.
[42] Campbell C A M, Pettersson J, Pickett J A, et al. Spring migration of damson-hop aphid, Phorodon humuli (Homoptera, Aphididae), and summer host plant-derived semiochemicals released on feeding[J]. Journal of Chemical Ecology, 1993, 19(7):1569-1576.
[43] Agrawal A A, Janssen A, Bruin J, et al. An ecological cost of plant defence:attractiveness of bitter cucumber plants to natural enemies of herbivores[J]. Ecology Letters, 2010, 5(3):377-385.
[44] Bruce T J A, Matthes M C, Chamberlain K, et al. cis-Jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids[J]. Proceedings of the National Academy of Sciences, 2008, 105(12):4553-4558.
[45] Kant M R, Ament K, Sabelis M W, et al. Differential timing of spider mite-induced direct and indirect defenses in tomato plants[J]. Plant Physiology, 2004, 135(1):483-495.
[46] Farrar R R, Kennedy G G. 2-Undecanone, a constituent of the glandular trichomes of Lycopersicon hirsutum f. glabratum:effects on Heliothis zea and Manduca sexta growth and survival[J]. Entomologia Experimentalis et Applicata. 1987, 43(1):17-23.
[47] Farrar R R, Kennedy G G, Roe R M. The protective role of dietary unsaturated fatty acids against 2-undecanone-induced pupal mortality and deformity in Helicoverpa zea[J]. Entomologia Experimentalis et Applicata, 1992, 62(2):191-200.
[48] Bruce T J, Birkett M A, Blande J, et al. Response of economically important aphids to components of Hemizygia petiolata essential oil[J]. Pest Management Science, 2005, 61(11):1115-1121.