Abstract
Tripartite plant–pathogen–phytophagous insect interactions have been widely studied. However, the effect of pathogens on phytophagous insects remains uncertain. Although alfalfa is a widely cultivated forage legume, Peronospora aestivalis and Therioaphis trifolii often co-occur in alfalfa, reducing quality and yields. To explore the relationships between alfalfa Zhongcao No. 3, P. aestivalis, and T. trifolii, an electrical penetration graph and four-arm olfactometer were used to determine T. trifolii behavior on infected and uninfected alfalfa. The physicochemical properties of infected alfalfa leaves were determined. The effects of volatiles on the selection behavior of T. trifolii were analyzed, and the effect of substance content on host selection behavior was determined. Peronospora aestivalis altered the nutrient composition of alfalfa, and T. trifolii preferentially fed on moderately infected alfalfa (P2) rather than severely infected alfalfa (P3). The E1 and E2 waveform durations were the shortest (11.87 min) and the longest in P2 (122.82 min), respectively. Therioaphis trifolii mostly chose moderately (25.71%) and severely (37.14%) infected alfalfa plants via olfaction. The analysis of volatile components revealed 53 substances in 8 categories. Among them, decanal (1×) and naphthalene (1000× and 10,000×) had a strong repellent effect on T. trifolii, whereas naphthalene (1×), cedrol (100×), 2,6,10,14,18,22-tetracosahexaene, 2,6,10,15,19,23- (1000× and 10,000×) attracted T. trifolii. Our results provide new insights into plant disease and insect pest control and prevention.
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References
Ammar ED, Walter AJ, Hall DG (2013) New excised-leaf assay method to test inoculativity of Asian citrus psyllid (hemiptera: psyllidae) with candidatus liberibacter asiaticus associated with citrus huanglongbing disease. J Econ EntomOl 106(1):25–35. https://doi.org/10.1603/ec12245
Baldrian P (2017) Forest microbiome: diversity, complexity and dynamics. FEMS Microbiol Rev 41:109–130. https://doi.org/10.1093/femsre/fuw040
Chen X, Liu YJ, Dong YH, Liu JY, Li W, Xu PJ, Zang Y, Ren GW (2021) Effects of CMV-infected tobacco on the performance, feeding and host selection behavior of Myzus persicae. Scientia Agricul Sin 54(8):1673–1683. https://doi.org/10.3864/j.issn.0578-1752.2021.08.008
Dai JQ, Han SC, Du JW (2010) Progress in stydies on behavioural effect of semiochemicals of host plant to insect. J Environ Entomo 32(3):407–414. https://doi.org/10.3969/j.issn.1674-0858.2010.03.020
Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the “cry for help.” Trends Plant Sci 15(3):167–175. https://doi.org/10.1016/j.tplants.2009.12.002
Edwards OR, Franzmann B, Thackray D, Micic S (2008) Insecticide resistance and implications for future aphid management in Australian grains and pastures: a review. Aust J Exp Agr 48:1523–1530. https://doi.org/10.1071/ea07426
Franziska E, Fernandez BM, Reichelt M, Hammerbacher A, Gershenzon J, Unsicker SB (2020) Herbivory meets fungivory: insect herbivores feed on plant pathogenic fungi for their own benefit. Ecol Lett 23(7):1073–1084. https://doi.org/10.1111/ele.13506
Hammerbacher A, Schmidt A, Wadke N, Wright LP, Schneider B, Bohlmann J (2013) A common fungal associate of the spruce bark beetle metabolizes the stilbene defenses of Norway spruce. Plant Physiol 162:1324–1336. https://doi.org/10.1104/pp.113.218610
He J, Zhou FC, Chen XH, Su HH, Yang AM, Heng S (2016) Effects of physical characteristics of pepper leaves on host selection of Bemisia tabaci. Chin J Ecol 35(11):3045–3050. https://doi.org/10.13292/j.1000-4890.201611.007
He YQ, Zhang YQ, Chen JN, Chen WL, Zeng XY, Chen HT, Ding W (2018) Effects of Aphidius gifuensis on the feeding behavior and potato virus Y transmission ability of Myzus persicae. Insect Sci 25(6):1025–1034. https://doi.org/10.1111/1744-7917.12476
Li JJ, Pan JB, Wu LL, Lu SH, Yan FM (2019) Three-decades of electrical penetration graph technique innovation in China. Chin J Appl Entomol 56(6):1224–1234. https://doi.org/10.7679/j.issn.2095-1353.2019.132
Li KM, Bo Z, Fang F (2008) Mensuration on resistance of alfalfa varieties to peronospora aestivalis in door. Acta Agric Sin 16(6):667–668. https://doi.org/CNKI:SUN:CDXU.0.2008-06-022
Li R, Weldegergis BT, Li J, Choonkyun J, Jing Q, Sun YW, Qian HM, Chuansia T, Joop JAL, Marcel D, Chua NH, Liu SS, Ye J (2014) Virulence factors of geminivirus interact with MYC2 to subvert plant resistance and promote vector performance. Plant Cell 26:4991–5008. https://doi.org/10.1105/tpc.114.133181
Liu JY, Liu YJ, Donkersley P, Dong YH, Chen X, Zang Y, Xu PJ, Ren GW (2019) Preference of the aphid Myzus persicae (Hemiptera: Aphididae) for tobacco plants at specific stages of potato virus Y infection. Arch Virol 164(6):1567–1573. https://doi.org/10.1007/s00705-019-04231-y
Luo GZ, Zou YH, Huo YZ (1990) Preliminary study on the mechanism of cucumber resistance induction: the relationship between soluble sugar content and lignin content in leaves and induced resistance. Acta Phytopath Sin. https://doi.org/10.13926/j.cnki.apps.1990.01.014
Mann RS, Ali JR, Hermann SL, Stelinski LL (2012) Induced release of a plant-defense volatile ‘Deceptively’ attracts insect vectors to pants infected with a bacterial pathogen. PLoS Pathog 8(3):1–13. https://doi.org/10.1371/journal.ppat.1002610
Mandadi KK, Scholthof KBG (2013) Plant immune responses against viruses: How does a virus cause disease? Plant Cell 25(5):1489–1505. https://doi.org/10.1105/tpc.113.111658
Martins DS, Ventura JA, Lima RCA, Culik MP, Costa H, Ferreirac PSF (2012) Interaction between Papaya meleira virus (PMeV) infection of papaya plants and Mediterranean fruit fly infestation of fruits. Crop Prot 36:7–10. https://doi.org/10.1016/j.cropro.2012.01.001
Masuda A, Akiyama S, Kuwano M, Ikekawa N (1982) Potentiation of antifungal effect of amphotericin B by squalene, an inter-mediate for sterol biosynthesis. J Antibiot 35(2):230–234. https://doi.org/10.7164/antibiotics.35.230
Nan ZB (2001) Alfalfa disease in my country and its integrated control system. Anim Sci Anim Med 4:81–84. https://doi.org/CNKI:SUN:TJXM.0.2001-04-047
Pope TW, Campbell C, Hardie J, Wadhams LJ (2004) Electroantennogram responses of the three migratory forms of the damson-hop aphid, phorodon humuli, to aphid pheromones and plant volatiles. J Insect Physiol 50(11):1083–1092. https://doi.org/10.1016/j.jinsphys.2004.09.010
Prasannakumar NR, Maruthi MN (2021) Understanding the interactions among the crop plants, a virus, insect vector whiteflies and their endosymbionts. Phytoparasitica 49:739–750. https://doi.org/10.1007/S12600-021-00905-Z
Reding ME, Alston DG, Thomson SV, Stark AV (2001) Association of powdery mildew and spider mite populations in apple and cherry orchards. Agr Ecosyst Environ 1662:1–10. https://doi.org/10.1016/S0167-8809(00)00204-8
Rostás M, Hilker M (2002) Asymmetric plant-mediated cross-effects between a herbivorous insect and a phytopathogenic fungus. Agric for Entomol 4(3):1–9. https://doi.org/10.1046/j.1461-9563.2002.00147.x
Russo VM, Russo BM, Peters M, Perkins-Veazie P, Cartwright B (1997) Interaction of colletotrichum orbiculare with thrips and aphid feeding on watermelon seedlings. Crop Prot 16:581–584. https://doi.org/10.1016/S0261-2194(97)00024-0
Stafford CA, Walker GP, Ullman DE (2011) Infection with a plant virus modifies vector feeding behavior. P Natl Acad Sci 108(23):9350–9355. https://doi.org/10.1073/pnas.1100773108
Sun QZ, Yu Z, Xu CC (2012) Urgency of further developing alfalfa industry in China. Pratacultural Sci 29(02):314–319. https://doi.org/CNKI:SUN:CYKX.0.2012-02-027
Van Wees SC, Van der Ent S, Pieterse CM (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448. https://doi.org/10.1016/j.pbi.2008.05.005
Wu X, Xu S, Zhao PZ, Zhang X, Yao XM, Sun YW, Fang RX, Ye J (2019) The Orthotospovirus nonstructural protein NSs suppresses plant MYC-regulated jasmonate signaling leading to enhanced vector attraction and performance. PloS Pathog 15(6):e1007897. https://doi.org/10.1371/journal.ppat.1007897
Wu WH (2018) Plant Physiology, 3rd edn. Science Press, Beijing. ISBN:9787030553188
Xue FX (2008) Grassland conservation—Volume 3—forage pathology. ISBN:9787109129672
Yan FS, Du YJ, Han XL (1994) Acomparative study on the electroantenogram responses of three aphid species to plant volatiles. Insect Sci 1(1):53–66. https://doi.org/10.1111/j.1744-7917.1994.tb00195.x
Yang SM, Gao MQ, Xu CW, Gao JC, Deshpande S, Lin SH, Roe BA, ZHU HY, (2008) Alfalfa benefits from medicago truncatula: the RCT1 gene from M. truncatula confers broad-spectrum resistance to anthracnose in alfalfa. Proc Natl Acad Sci USA 105(34):12164–12169. https://doi.org/10.1073/pnas.0802518105
Ye J, Gong YQ, Fang RX (2017) Research progress and perspective of tripartite interaction of virus-vector-plant in vector-borne viral diseases. Bull Chin Acad Sci 32(8):845–855. https://doi.org/10.16418/j.issn.1000-3045.2017.08.006
Zieglfr H (1990) Detoxification of humans and animals with squalane and squalene. DE Patent: 4 017 172, 1990-12-20
Zhao JM (2017) Common diseases and pests of alfalfa and green prevention technology. Chin Cattl Sci 43(03):46–48. https://doi.org/CNKI:SUN:BULL.0.2017-03-014
Acknowledgements
We thank Professor Li Kemei of Xinjiang Agricultural University for her support in designing the method for the inoculation of P. aestivalis.
Funding
This study was supported by the Inner Mongolia Science and Technology Plan (2020GG0141) and the Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (1610332011009, 161033201214, 1610332013008).
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Yu, L., Lin, K., Xu, L. et al. Downy mildew (Peronospora aestivalis) infection of alfalfa alters the feeding behavior of the aphid (Therioaphis trifolii) and the chemical characteristics of alfalfa. J Pest Sci 96, 989–1001 (2023). https://doi.org/10.1007/s10340-022-01571-8
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DOI: https://doi.org/10.1007/s10340-022-01571-8