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Interference mechanism of Sophora alopecuroides L. alkaloids extract on host finding and selection of the Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae)

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Abstract

Manipulating insect behavior through the deployment of semiochemicals offers a promising opportunity for protecting crops in a sustainable manner. Therefore, there is still a significant opportunity for the development of natural crop protectants as eco-friendly tools in pest management. In this context, the aim of the current investigation is to find a novel prophylactic against the Asian citrus psyllid (ACP) and to gain a better understanding of the host-finding and selection ability of the ACP towards Murraya paniculata seedlings treated with Sophora alopecuroides alkaloids extract (SAAE). Our results indicate that foliar application of SAAE influences the psyllid host-finding and selection process. The behavioral assay with M. paniculata seedlings treated with 15 and 30 mg/mL of SAAE, with masked visual cues, revealed that only 6.6 and 10.4% psyllids were able to locate the host in the vials. The results also indicate that citrus psyllids mainly rely on both visual and olfaction in host-finding and selection. In choice settling experiments, psyllids settled almost completely on control seedlings rather than on seedlings treated with SAAE at a concentration of 30 mg/mL. Chemical analyses of the alkaloids extract revealed the presence of sophocarpine (33.90%), sophoridine (6.23%), anagyrine (2.77%), matrine (2.38%), lupanine (1.68%) aphylline (0.89%), and sophoramine (0.75%). In further behavioral bioassays with the dominant alkaloids sophocarpine and sophoridine, the alkaloids repelled ACP at higher concentrations of 50 and 70 mg/mL as compared to SAAE. Furthermore, the 50 mg/mL (1:1, v/v) combination of sophocarpine and sophoridine displayed a synergistic effect and showed the maximum behavioral effect as compared to the individual alkaloid. Based on our results, SAAE makes M. paniculata seedlings unattractive to the psyllids, and therefore, alkaloids could be used in reducing the colonization of citrus plants, subsequently curtailing HLB infection.

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References

  • Alquezar B et al (2017) β-Caryophyllene emitted from a transgenic arabidopsis or chemical dispenser repels Diaphorina citri, vector of Candidatus liberibacters. Sci Rep 7:5639

    Article  CAS  Google Scholar 

  • Anaya-Eugenio GD, Bye R-C, Linares I, Mata ER (2016) Antinociceptive activity of the essential oil from Artemisia ludoviciana. J Ethnopharmacol 179:403–411

    Article  CAS  Google Scholar 

  • Bano A et al (2014) Quantitative ethnomedicinal study of plants used in the skardu valley at high altitude of Karakoram-Himalayan range, Pakistan. J Ethnobiol Ethnomed 10:43–51

    Article  Google Scholar 

  • Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils a review. Food Chem Toxicol 46:446–475

    Article  CAS  Google Scholar 

  • Barman JC, Zeng X (2014) Effect of Guava Leaf Extract on Citrus Attractiveness to Asian Citrus Psyllid Diaphorina citri Kuwayama Pakistan Journal of Zoology 46:1117–1124

  • Barman JC, Campbell SA, Zeng X (2016) Exposure to guava affects citrus olfactory cues and attractiveness to Diaphorina citri (Hemiptera: Psyllidae). Environ Entomol 45:694–699

    Article  Google Scholar 

  • Baxter CV, Kennedy TA, Miller SW, Muehlbauer JD, Smock LA (2017) Macroinvertebrate drift, adult insect emergence and oviposition. Methods in stream ecology, volume 1 (third edition). Elsevier, pp 435–456

  • Benelli G, Govindarajan M, Rajeswary M, Vaseeharan B, Alyahya SA, Alharbi NS, Kadaikunnan S, Khaled JM, Maggi F (2018) Insecticidal activity of camphene, zerumbone and α-humulene from Cheilocostus speciosus rhizome essential oil against the Old-World bollworm, Helicoverpa armigera. Ecotoxicology and Environmental Safety 148:781–786

  • Ben-Issa R, Gomez L, Gautier H (2017) Companion plants for aphid. Pest Manag Sci 8:112–121

    Google Scholar 

  • Bermudez-Torres K, Herrera JM, Brito RF, Wink M, Legal L (2009) Activity of quinolizidine alkaloids from three Mexican lupinus against the lepidopteran crop pest Spodoptera frugiperda. Biol Control 54:459–466

    CAS  Google Scholar 

  • Brem B, Seger C, Pacher T, Hofer O, Vajrodaya S, Greger H (2002) Feeding deterrence and contact toxicity of Stemona alkaloids a source of potent natural insecticides. J Agr Food Chem 50:6383–6388

    Article  CAS  Google Scholar 

  • Bruce TJ, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects–finding the right mix. Phytoche 72:1605–1611

    Article  CAS  Google Scholar 

  • Bruce TJ, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274

    Article  CAS  Google Scholar 

  • Byrne FJ, Daugherty MP, Grafton-Cardwell EE, Bethke JA, Morse JG (2017) Evaluation of systemic neonicotinoid insecticides for the management of the Asian citrus psyllid Diaphorina citri on containerized citrus. Pest Manag Sci 73:506–514

    Article  CAS  Google Scholar 

  • Cai Q-N, Han Y, Cao Y-Z, Hu Y, Zhao X, Bi J-L (2009) Detoxification of gramine by the cereal aphid Sitobion avenae. J Chem Ecol 35:320–325

    Article  CAS  Google Scholar 

  • Cai Q, Zhang Q, Cheo M (2004) Contribution of indole alkaloids to Sitobion avenae (F.) resistance in wheat. J Appl Entomol 128:517–521

    Article  CAS  Google Scholar 

  • Chen XD, Seo M, Stelinski LL (2017) Behavioral and hormetic effects of the butenolide insecticide, flupyradifurone, on Asian citrus psyllid, Diaphorina citri. Crop Prot 98:102–107

    Article  CAS  Google Scholar 

  • Choudhary MI, Parvez K, Ahmed A, Akhtar F, Nur-e-Alam M, Hassan NM (2000) Quinolizidine alkaloids from Sophora alopecuroides. J Nat Prod 63:190–192

    Article  CAS  Google Scholar 

  • Hall DG, Borovsky D, Chauhan KR, Shatters RG (2018) An evaluation of mosquito repellents and essential plant oils as deterrents of Asian citrus psyllid. Crop Prot 108:87–94

    Article  CAS  Google Scholar 

  • Davis P, Plitmann U (1970) Vicia In: Davis, PH (ed.), Flora of Turkey 3: 274–325. Edinburgh university press Edinburgh

  • De Bruyne M, Baker T (2008) Odor detection in insects: volatile codes. J Chem Ecol 34:882–897

    Article  CAS  Google Scholar 

  • Fancelli M, Borges M, Laumann RA, Pickett JA, Birkett MA, Blassioli-Moraes MC (2018) Attractiveness of Host Plant Volatile Extracts to the Asian Citrus Psyllid, Diaphorina citri, is Reduced by Terpenoids from the Non-Host Cashew. Journal of Chemical Ecology 44(4):397–405

  • Finch S, Collier R (2000) Host-plant selection by insects–a theory based on ‘appropriate/inappropriate landings’ by pest insects of cruciferous plants. Entomol Exp Appl 96:91–102

    Article  Google Scholar 

  • Feitosa-Alcantara RB et al (2017) Essential oils of Hyptis pectinata chemotypes: isolation, binary mixtures and acute toxicity on leaf-cutting ants. Molecules 22:621–631

    Article  CAS  Google Scholar 

  • Gao HY, Li GY, Wang JH (2012) A new alkaloid from the seeds of Sophora alopecuroides L. Helv Chim Act 95:1108–1113

    Article  CAS  Google Scholar 

  • Garcia BA et al. (2017) Repellent compositions and genetic approaches for controlling huanglongbing. Google Patents US 9,572,349 B2

  • Goggin FL (2007) Plant–aphid interactions: molecular and ecological perspectives. Curr Opin Plant Biol 10:399–408

    Article  CAS  Google Scholar 

  • Halbert SE, Manjunath KL (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Fla Entomol 87:330–353

    Article  Google Scholar 

  • Hall DG, Rohrig E (2015) Bionomics of Asian citrus psyllid (Hemiptera: Liviidae) associated with orange jasmine hedges in southeast central Florida, with special reference to biological control by Tamarixia radiata. J Econ Entomol 108:1198–1207

    Article  Google Scholar 

  • Jinbo Z, Mingan W, Wenjun W, Zhiqing J, Zhaonong H (2002) Insecticidal sesquiterpene pyridine alkaloids from euonymus species. Phytochem 61:699–704

    Article  Google Scholar 

  • Kanga LH, Eason J, Haseeb M, Qureshi J, Stansly P (2016) Monitoring for insecticide resistance in Asian citrus psyllid (Hemiptera: Psyllidae) populations in Florida. J Econ Entomol 109:832–836

    Article  CAS  Google Scholar 

  • Kucukboyaci N, Ozkan S, Adiguzel N, Tosun F (2011) Characterisation and antimicrobial activity of Sophora alopecuroides L. var alopecuroides alkaloid extracts. Turk J Biol 35:379–385

    CAS  Google Scholar 

  • Kwon J, Basnet S, Lee JW, Seo E-K, Tsevegsuren N, Hwang BY, Lee D (2015) Chemical constituents isolated from the Mongolian medicinal plant Sophora alopecuroides L. and their inhibitory effects on LPS-induced nitric oxide production in RAW 264.7 macrophages. Bioorg Med Chem Lett 25:3314–3318

    Article  CAS  Google Scholar 

  • Leather SR (2018) Factors affecting fecundity, fertility, oviposition, and larviposition in insects. In: Insect reproduction. Crc Press, pp 143–174

  • Liu L, Alam MS, Hirata K, Matsuda K, Ozoe Y (2008) Actions of quinolizidine alkaloids on Periplaneta americana nicotinic acetylcholine receptors. Pest Manag Sci 64:1222–1228

    Article  CAS  Google Scholar 

  • Liu ZL, Liu QZ, Du SS, Deng ZW (2012) Mosquito larvicidal activity of alkaloids and limonoids derived from Evodia rutaecarpa unripe fruits against Aedes albopictus (Diptera: Culicidae). Parasitol Res 111:991–996

    Article  Google Scholar 

  • Lopez-Gresa MP, Gonzalez MC, Ciavatta L, Ayala I, Moya P, Primo J (2006) Insecticidal activity of paraherquamides, including paraherquamide H and paraherquamide I, two new alkaloids isolated from Penicillium cluniae. J Agr Food Chem 54:2921–2925

    Article  CAS  Google Scholar 

  • Lu P-F, Huang L-Q, Wang C-Z (2012) Identification and field evaluation of pear fruit volatiles attractive to the oriental fruit moth, Cydia molesta. J Chem Ecol 38:1003–1016

    Article  Google Scholar 

  • Lu Y, Hu R, Pan Y (2010) Integrated countercurrent extraction of natural products: a combination of liquid and solid supports. Anal Chem 82:3081–3085

    Article  CAS  Google Scholar 

  • Lu Z-G, Li M-H, Wang J-S, Wei D-D, Liu Q-W, Kong L-Y (2014) Developmental toxicity and neurotoxicity of two matrine-type alkaloids, matrine and sophocarpine, in zebrafish (Danio rerio) embryos/larvae. Reprod Toxicol 47:33–41

    Article  CAS  Google Scholar 

  • Ma T, Yan H, Shi X, Liu B, Ma Z, Zhang X (2018) Comprehensive evaluation of effective constituents in total alkaloids from Sophora alopecuroides L. and their joint action against aphids by laboratory toxicity and field efficacy. Ind Crop Prod 111:149–157

    Article  CAS  Google Scholar 

  • Ma X, xx L, Zhang QW, Zhao JZ, Cai QN, Ma YA, Chen DM (2006) Assessment of cotton aphids, Aphis gossypii, and their natural enemies on aphid-resistant and aphid-susceptible wheat varieties in a wheat–cotton relay intercropping system. Entomol Exp Appl 121:235–241

    Article  Google Scholar 

  • Mann R, Rouseff R, Smoot J, Castle W, Stelinski L (2011) Sulfur volatiles from Allium spp. affect Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), response to citrus volatiles. B Entomol Res 101:89–97

    Article  CAS  Google Scholar 

  • Mauchline AL, Osborne JL, Martin AP, Poppy GM, Powell W (2005) The effects of non-host plant essential oil volatiles on the behaviour of the pollen beetle Meligethes aeneus. Entomol Exp Appl 114:181–188

    Article  CAS  Google Scholar 

  • Meng X, Hu J, Li Y, Dai J, Guo M, Ouyang G (2018) The preference choices of Conopomorpha sinensis Bradley (Lepidoptera: Gracilariidae) for litchi based on its host surface characteristics and volatiles. Sci Rep 8:2013

    Article  CAS  Google Scholar 

  • Mukherjee A, Sarkar N, Barik A (2015) Momordica cochinchinensis (Cucurbitaceae) leaf volatiles: semiochemicals for host location by the insect pest, Aulacophora foveicollis (Coleoptera: Chrysomelidae). Chemoecology 25:93–104

    Article  CAS  Google Scholar 

  • Najar-Rodriguez AJ, Galizia CG, Stierle J, Dorn S (2011) Behavioural and neurophysiological responses of an insect to changing ratios of constituents in host plant-derived volatile mixtures. J Exp Biol 214:162–162

    Article  Google Scholar 

  • Nerio LS, Olivero-Verbel J, Stashenko E (2010) Repellent activity of essential oils: a review. Bioresour Technol 101:372–378

    Article  CAS  Google Scholar 

  • Obomanu F, Ogbalu O, Gabriel U, Fekarurhobo G, Adediran B (2006) Larvicidal properties of Lepidagathis alopecuroides and Azadirachta indica on Anopheles gambiae and Culex quinquefasciatus. African J Biotec 5:761–765

    Google Scholar 

  • Onagbola E, Rouseff R, Smoot J, Stelinski L (2011) Guava leaf volatiles and dimethyl disulphide inhibit response of Diaphorina citri Kuwayama to host plant volatiles. J Appl Entomol 135:404–414

    Article  Google Scholar 

  • Park B-S, Lee S-E, Choi W-S, Jeong C-Y, Song C, Cho K-Y (2002) Insecticidal and acaricidal activity of pipernonaline and piperoctadecalidine derived from dried fruits of Piper longum L. Crop Prot 21:249–251

    Article  CAS  Google Scholar 

  • Pavela R, Sedlak P (2018) Post-application temperature as a factor influencing the insecticidal activity of essential oil from Thymus vulgaris. Ind Crop Prod 113:46–49

    Article  CAS  Google Scholar 

  • Pickett J, Wadhams L, Woodcock C, Hardie J (1992) The chemical ecology of aphids. Annu Rev Entomol 37:67–90

    Article  CAS  Google Scholar 

  • Poelman EH et al (2012) Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLoS Biol 10:e1001435

    Article  CAS  Google Scholar 

  • Poelman EH, Dicke M (2018) Plant-mediated interactions among insects within a community ecological perspective. Annual Plant Reviews: pp 309–337

  • Quitain AT, Ozturk B, Mission EG, Sasaki M (2018) Microwave-assisted pressurized hot water extraction of alkaloids. In: Water extraction of bioactive compounds. Elsevier, pp 269–289

  • Renwick J (1989) Chemical ecology of oviposition in phytophagous insects. Experientia 45:223–228

    Article  CAS  Google Scholar 

  • Tian F, Mo X, Rizvi SAH, Li C, Zeng X (2018) Detection and biochemical characterization of insecticide resistance in field populations of Asian citrus psyllid in Guangdong of China. Sci Rep 8:12587

    Article  CAS  Google Scholar 

  • Rizvi SAH, Siquan L, Fajun T, Feng X, Xinnian Z (2018) Toxicity and enzyme inhibition activities of the essential oil and dominant constituents derived from Artemisia absinthium L. against adult Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae). Ind Crop Prod 121:468–475

    Article  CAS  Google Scholar 

  • Rouseff RL, Onagbola EO, Smoot JM, Stelinski LL (2008) Sulfur volatiles in guava (Psidium guajava L.) leaves: possible defense mechanism. J Agr Food Chem 56:8905–8910

    Article  CAS  Google Scholar 

  • Ruan C-Q, Hall DG, Liu B, Duan Y-P, Li T, Hu H-Q, Fan G-C (2015) Host-choice behavior of Diaphorina citri Kuwayama (Hemiptera: Psyllidae) under laboratory conditions. J Insect Beh 28:138–146

    Article  Google Scholar 

  • Schlaeger S, Pickett JA, Birkett MA (2018) Prospects for management of whitefly using plant semiochemicals, compared with related pests. Pest Manag Sci. https://doi.org/10.1002/PS5058

  • Silva JA et al (2016) Repellency of selected Psidium guajava cultivars to the Asian citrus psyllid, Diaphorina citri. Crop Prot 84:14–20

    Article  Google Scholar 

  • Srinivasan R, Hoy MA, Singh R, Rogers ME (2008) Laboratory and field evaluations of Silwet L-77 and kinetic alone and in combination with imidacloprid and abamectin for the management of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Fla Entomol 91:87–100

    Article  CAS  Google Scholar 

  • Sun ZL, He JM, Lan JE, Mu Q (2017) High-speed counter-current chromatography with an online storage technique for the preparative isolation and purification of dihydroflavonoids from Sophora alopecuroides L. Phytochem Analysis 28:496–504

    Article  CAS  Google Scholar 

  • Tiwari S, Lewis-Rosenblum H, Pelz-Stelinski K, Stelinski LL (2010) Incidence of Candidatus Liberibacter asiaticus infection in abandoned citrus occurring in proximity to commercially managed groves. J Econ Entomol 103:1972–1978

    Article  Google Scholar 

  • Wang H, Guo S, Qian D, Qian Y, J-a D (2012) Comparative analysis of quinolizidine alkaloids from different parts of Sophora alopecuroides seeds by UPLC–MS/MS. J Pharmaceut Biomed 67:16–21

    Article  CAS  Google Scholar 

  • Wenninger EJ, Stelinski LL, Hall DG (2008) Behavioral evidence for a female-produced sex attractant in Diaphorina citri. Entomol Exp Appl 128:450–459

    Article  Google Scholar 

  • Wink M (2018) Plant secondary metabolites modulate insect behavior-steps toward addiction? Front Physiol 9:364–371

    Article  Google Scholar 

  • Witten IH, Frank E, Hall MA, Pal CJ (2016) Data mining: practical machine learning tools and techniques. Morgan Kaufmann, Elsevier 50 hampshire street, 5th floor, Cambridge, MA 02139, USA

  • Wood CW, Wice EW, del Sol J, Paul S, Sanderson BJ, Brodie ED III (2018) Constraints imposed by a natural landscape override offspring fitness effects to shape oviposition decisions in wild forked fungus beetles. Am Nat 191:524–538

    Article  Google Scholar 

  • Zaka SM, Zeng X, Holford P, Beattie GAC (2010) Repellent effect of guava leaf volatiles on settlement of adults of citrus psylla, Kuwayama, on citrus . Insect Science 17(1):39–45

  • Zaka SM, Zeng X, Wang H (2015) Chemotaxis of adults of the asiatic citrus psyllid, Diaphorina citri Kuwayama, to volatile terpenes detected from guava leaves. Pak J Zoo 47:153–159

    CAS  Google Scholar 

  • Zhang QH, Schlyter F (2004) Olfactory recognition and behavioural avoidance of angiosperm nonhost volatiles by conifer-inhabiting bark beetles. Agr Forest Entomol 6:1–20

    Article  CAS  Google Scholar 

  • Zhang Y-B, Zhang X-L, Chen N-H, Wu Z-N, Ye W-C, Li Y-L, Wang G-C (2017) Four matrine-based alkaloids with antiviral activities against HBV from the seeds of Sophora alopecuroides. Org Lett 19:424–427

    Article  CAS  Google Scholar 

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Acknowledgments

Thanks are due to the National Key R&D Program of China (2017YFD0202005), the Natural Science Foundation of China (31572314), and the Department of Science and Technology of Guangdong Province (2015B090903076) for the financial support to the present research.

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  1. Guangdong Engineering Research Center for Insect Behavior Regulation, College of Agriculture, South China Agricultural University, Guangzhou, 510642, China

    Syed Arif Hussain Rizvi, Siquan Ling, Fajun Tian, Jiali Liu & Xinnian Zeng

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  1. Syed Arif Hussain Rizvi
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  2. Siquan Ling
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  3. Fajun Tian
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  4. Jiali Liu
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Conceived, designed, and performed the experiments: SAHR, ZX, and JL gives the direction of research and reviewed the manuscript, SL and FT help in analyzing the manuscript.

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Correspondence to Xinnian Zeng.

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Rizvi, S.A.H., Ling, S., Tian, F. et al. Interference mechanism of Sophora alopecuroides L. alkaloids extract on host finding and selection of the Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae). Environ Sci Pollut Res 26, 1548–1557 (2019). https://doi.org/10.1007/s11356-018-3733-0

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