Barley yellow dwarf virus-infected wheat plant modulated selection behavior of vector aphids

Zhengqiang Hu1, Ruirui Chai1, Xin Liu1, Yao Dong1, Dan Su1, Nicolas Desneux2, Xiaoling Tan3, Chen Luo1
1State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University, Yangling, 712100, Shaanxi Province, China
2Université Côte d’Azur, INRAE, CNRS, UMR ISA, 06000 Nice, France
3State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China

Tóm tắt

Từ khóa


Tài liệu tham khảo

Achhami BB, Reddy G, Hofland ML, Sherman JD, Peterson R, Weaver DK (2021) Plant volatiles and oviposition behavior in the selection of barley cultivars by wheat stem sawfly (Hymenoptera: Cephidae). Environ Entomol 50:940–947. https://doi.org/10.1093/ee/nvab035

Ajayi O, Dewar AM (1983) The effect of Barley yellow dwarf virus on field populations of the cereal aphids, Sitobion avenae and Metopolophium dirhodum. Ann Appl Biol 103:1–11. https://doi.org/10.1111/j.1744-7348.1983.tb02734.x

Belliure B, Janssen A, Maris PC, Peters D, Sabelis MW (2005) Herbivore arthropods benefit from vectoring plant viruses. Ecol Lett 8:70–79. https://doi.org/10.1111/j.1461-0248.2004.00699.x

Bocca FM, Picciau L, Alma A (2020) New insights on Scaphoideus titanus biology and their implications for integrated pest management. Entomol Gen 40:337–349. https://doi.org/10.1127/entomologia/2020/0977

Boquel S, Delayen C, Couty A, Giordanengo P, Ameline A (2012) Modulation of aphid vector activity by Potato virus Y on in vitro potato plants. Plant Dis 96:82–86. https://doi.org/10.1094/PDIS-06-11-0499

Cantelo WW, Jacobson M (1979) Phenylacetaldehyde attracts moths to bladder flower and to blacklight traps. Environ Entomol 8:444–447. https://doi.org/10.1093/ee/8.3.444

Carmo-Sousa M, Moreno A, Plaza M, Garzo E, Fereres A (2016) Cucurbit aphid-borne yellows virus (CABYV) modifies the alighting, settling and probing behaviour of its vector Aphis gossypii favouring its own spread. Ann Appl Biol 169:284–297. https://doi.org/10.1111/aab.12300

Castle SJ, Berger PH (1993) Rates of growth and increase of Myzus persicae on virus-infected potatoes according to type of virus-vector relationship. Entomol Exp Appl 69:51–60. https://doi.org/10.1111/j.1570-7458.1993.tb01727.x

Chen JL, Ni HX, Ding HJ, Sun JR (2000) Studies on a chemically defined diet of English grain aphid. Scientia Agricultura Sinica 33(3):54–59 (in Chinese)

Chen G, Su Q, Shi Xb, Liu X, Peng ZK et al (2017) Odor, not performance, dictates Bemisia tabaci’s selection between healthy and virus infected plants. Front Physiol 8:146. https://doi.org/10.3389/fphys.2017.00146

Chung SH, Parker BJ, Blow F, Brisson JA, Douglas AE (2020) Host and symbiont genetic determinants of nutritional phenotype in a natural population of the pea aphid. Mol Ecol 29:848–858. https://doi.org/10.1111/mec.15355

Cornara D, Morente M, Markheiser A, Bodino N, Tsai CW, Fereres A et al (2019) An overview on the worldwide vectors of Xylella fastidiosa. Entomol Gen 39:157–181. https://doi.org/10.1127/entomologia/2019/0811

Döring TF, Chittka L (2007) Visual ecology of aphids—a critical review on the role of colours in host finding. Arthropod-Plant Interact 1:3–16. https://doi.org/10.1007/s11829-006-9000-1

Eigenbrode SD, Bosque-Pérez NA (2016) Chemical ecology of aphid-transmitted plant viruses. In: Brown JK (ed) Vector-mediated transmission of plant pathogens. APS Press, St. Paul, MN, pp 3–19

Eigenbrode SD, Ding H, Shiel P, Berger PH (2002) Volatiles from potato plants infected with Potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc R Soc Lond B 269:455–460. https://doi.org/10.1098/rspb.2001.1909

Fereres A, Penaflor MFGV, Favaro CF, Azevedo KEX, Landi CH, Maluta NKP et al (2016) Tomato infection by whitefly transmitted circulative and non-circulative viruses induce contrasting changes in plant volatiles and vector behaviour. Viruses 8:225–240. https://doi.org/10.3390/v8080225

Fereres A, Moreno A (2009) Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Res 141:158–168. https://doi.org/10.1016/j.virusres.2008.10.020

Fingu-Mabola JC, Martin C, Bawin T, Verheggen FJ, Francis F (2020) Does the infectious status of aphids influence their preference towards healthy, virus-infected and endophytically colonized plants? Insects 11:435. https://doi.org/10.3390/insects11070435

Fujii T, Hori M, Matsuda K (2010) Attractants for rice leaf bug, Trigonotylus caelestialium (Kirkaldy), are emitted from flowering rice panicles. J Chem Ecol 36:999–1005. https://doi.org/10.1007/s10886-010-9839-6

Gildow FE, Rochow WF (1983) Barley yellow dwarf in California: vector competence and luteovirus identification. Plant Dis 67:140–143. https://doi.org/10.1094/PD-67-140

Hu ZQ, Zhao HY, Thieme T (2014) Comparison of the potential rate of population increase of brown and green color morphs of Sitobion avenae (Homoptera: Aphididae) on barley infected and uninfected with Barley yellow dwarf virus. Insect Sci 21:326–333. https://doi.org/10.1111/1744-7917.12084

Hulle M, Chaubet B, Turpeau E, Simon JC (2020) Encyclop’Aphid: a website on aphids and their natural enemies. Entomol Gen 40:97–101. https://doi.org/10.1127/entomologia/2019/0867

Ingwell LL, Eigenbrode SD, Bosque-Pérez NA (2012) Plant viruses alter insect behavior to enhance their spread. Sci Rep 2:578. https://doi.org/10.1038/srep00578

James DG (2005) Further field evaluation of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. J Chem Ecol 31:481–495. https://doi.org/10.1007/s10886-005-2020-y

Jiménez-Martínez ES, Bosque-Pérez NA, Berger PH, Zemetra RS (2004a) Life history of the bird cherry-oat aphid, Rhopalosiphum padi (Homoptera: Aphididae), on transgenic and untransformed wheat challenged with Barley yellow dwarf virus. J Econ Entomol 97:203–212. https://doi.org/10.1603/0022-0493-97.2.203

Jiménez-Martínez ES, Bosque-Pérez NA, Berger PH, Zemetra RS, Ding H, Eigenbrode SD (2004b) Volatile cues influence the response of Rhopalosiphum padi (Homoptera: Aphididae) to Barley yellow dwarf virus-infected transgenic and untransformed wheat. Environ Entomol 33:1207–1216. https://doi.org/10.1603/0046-225X-33.5.1207

Khanzada MS, Wang S, Huang NX, Pang H, Tan XL, Khanzada SR (2019) Optimization of microencapsulated artificial diets for mass rearing of the predacious big eyed bug, Geocoris pallidipennis. Entomol Gen 39:353–363. https://doi.org/10.1127/entomologia/2019/0478

Legarrea S, Barman A, Marchant W, Diffie S, Srinivasan R (2015) Temporal effects of a Begomovirus infection and host plant resistance on the preference and development of an insect vector, Bemisia tabaci, and implications for epidemics. PLoS ONE 10:e0142114. https://doi.org/10.1371/journal.pone.0142114

Li DD, Su D, Tong ZQ, Zhang C, Zhang GS, Zhao HY et al (2019) Virus-dependent and -independent responses of Sitobion avenae (Homoptera: Aphididae) feeding on wheat infected by transmitted and nontransmitted viruses at transcriptomic level. J Econ Entomol 112:2067–2076. https://doi.org/10.1093/jee/toz162

Li DD, Zhang C, Tong ZQ, Su D, Zhang GS, Zhao HY et al (2020) Transcriptome response comparison between vector and non-vector aphids after feeding on virus-infected wheat plants. BMC Genomics 21:638. https://doi.org/10.1186/s12864-020-07057-0

Liu Y, Sun B, Wang XF, Zheng CL, Zhou GH (2007) Three digoxigenin-labeled cDNA probes for specific detection of the natural population of Barley yellow dwarf viruses in China by dot-blot hybridization. J Virol Methods 145:22–29. https://doi.org/10.1016/j.jviromet.2007.05.006

Liu B, Preisser EL, Chu D, Pan H, Xie W, Wang S et al (2013) Multiple forms of vector manipulation by a plant-infecting virus: Bemisia tabaci and Tomato yellow leaf curl virus. J Virol 87:4929–4937. https://doi.org/10.1128/JVI.03571-12

Liu JH, Zhao XJ, Zhan YD, Wang K, Francis F, Liu Y (2021) New slow release mixture of (E)-β-farnesene with methyl salicylate to enhance aphid biocontrol efficacy in wheat ecosystem. Pest Manag Sci 77:3341–3348. https://doi.org/10.1002/ps.6378

Luan JB, Wang XW, Colvin J, Liu SS (2014) Plant-mediated whitefly–begomovirus interactions: research progress and future prospects. Bull Entomol Res 104:267–76. https://doi.org/10.1017/S000748531400011X

Luo C, Gatti JL, Monticelli LS, Poirié M, Desneux N, Zhao HY et al (2020a) An increased risk of parasitism mediated by the facultative symbiont Regiella insecticola. J Pest Sci 93:737–745. https://doi.org/10.1007/s10340-019-01189-3

Luo C, Monticelli LS, Li DD, Ahmed SS, Pandharikar G, Zhao HY et al (2020b) Comparison of life-history traits and resistance for Sitobion avenae (Fabricius) harboring a facultative symbiont. Entomol Gen 40:39–47. https://doi.org/10.1127/entomologia/2019/0823

Mann RS, Sidhu JS, Butter NS (2009) Settling preference of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) on healthy versus Cotton leaf curl virus-infected cotton plants. Int J Trop Insect Sci 29:57–61. https://doi.org/10.1017/S1742758409990142

Markheiser A, Cornara D, Fereres A, Maixner M (2020) Analysis of vector behavior as a tool to predict Xylella fastidiosa patterns of spread. Entomol Gen 40:1–13. https://doi.org/10.1127/entomologia/2019/0841

Mauck KE, De Moraes CM, Mescher MC (2010) Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. P Natl Acad Sci USA 107:3600–3605. https://doi.org/10.1073/pnas.0907191107

Mauck K, Bosque-Pérez NA, Eigenbrode SD, De Moraes CM, Mescher MC (2012) Transmission mechanisms shape pathogen effects on host-vector interactions: evidence from plant viruses. Funct Ecol 26:1162–1175. https://doi.org/10.1111/j.1365-2435.2012.02026.x

Mayer CJ, Vilcinskas A, Gross J (2008) Phytopathogen lures its insect vector by altering host plant odor. J Chem Ecol 34:1045–1049. https://doi.org/10.1007/s10886-008-9516-1

Mcelhany P, Real LA, Power AG (1995) Vector preference and disease dynamics: A study of Barley yellow dwarf virus. Ecology 76:444–457. https://doi.org/10.2307/1941203

Mckenzie C (2002) Effect of Tomato mottle virus (ToMoV) on Bemisia tabaci biotype B (Homoptera:Aleyrodidae) oviposition and adult survivorship on healthy tomato. Fla Entomol 85:367–368. https://doi.org/10.1653/0015-4040(2002)085[0367:EOTMVT]2.0.CO;2

Medina-Ortega K, Bosque-Pérez NA, Ngumbi E, Jiménez-Martínez ES, Eigenbrode SD (2009) Rhopalosiphum padi (Hemiptera: Aphididae) responses to volatile cues from Barley yellow dwarf virus-infected wheat. Environ Entomol 38:836–845. https://doi.org/10.1603/022.038.0337

Montllor CB, Gildow FE (1986) Feeding responses of two grain aphids to Barley yellow dwarf virus infected oats. Entomol Exp Appl 42:63–69. https://doi.org/10.1111/j.1570-7458.1986.tb02188.x

Moreno-Delafuente A, Garzo E, Moreno A, Fereres A (2013) A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread. PLoS ONE 8:e61543. https://doi.org/10.1371/journal.pone.0061543

Ngumbi E, Eigenbrode SD, Bosque-Pérez NA, Ding H, Rodriguez A (2007) Myzus persicae is arrested more by blends than by individual compounds elevated in headspace of PLRV-infected potato. J Chem Ecol 33:1733–1747. https://doi.org/10.1007/s10886-007-9340-z

Palmer LJ, Stangoulis JCR (2018) Changes in the elemental and metabolite profile of wheat phloem sap during grain filling indicate a dynamic between plant maturity and time of day. Metabolites 8:53. https://doi.org/10.3390/metabo8030053

Pan HP, Chu D, Liu BM, Shi XB, Guo LT, Xie W et al (2013) Differential effects of an exotic plant virus on its two closely related vectors. Sci Rep 3:2230. https://doi.org/10.1038/srep02230

R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

Rajabaskar D, Bosque-Pérez NA, Eigenbrode SD (2014) Preference by a virus vector for infected plants is reversed after virus acquisition. Virus Res 186:32–37. https://doi.org/10.1016/j.virusres.2013.11.005

Srinivasan R, Alvarez JM, Eigenbrode SD, Bosque-Perez NA (2006) Influence of hairy nightshade Solanum sarrachoides (Sendtner) and Potato leafroll virus (Luteoviridae: Polerovirus) on the host preference of Myzus persicae (Sulzer) (Homoptera: Aphididae). Environ Entomol 35:546–553. https://doi.org/10.1603/0046-225X-35.2.546

Su Q, Preisser EL, Zhou XM, Xie W, Liu BM, Wang WK et al (2015) Manipulation of host quality and defense by a plant virus improves performance of whitefly vectors. J Econ Entomol 108:11–19. https://doi.org/10.1093/jee/tou012

Su Q, Mescher MC, Wang SL, Chen G, Xie W, Wu QJ et al (2016) Tomato yellow leaf curl virus differentially influences plant defence responses to a vector and a non-vector herbivore. Plant Cell Environ 39:597–607. https://doi.org/10.1111/pce.12650

Tan XL, Chen JL, Benelli G, Desneux N, Yang XQ, Liu TX et al (2017) Pre-infestation of tomato plants by aphids modulates transmission-acquisition relationship among whiteflies, tomato yellow leaf curl virus (TYLCV) and plants. Front Plant Sci 8:1597. https://doi.org/10.3389/fpls.2017.01597

Urbaneja-Bernat P, Carrillo D, Jaques JA (2020) Behavior of Diaphorina citri: an investigation of the potential risk to the most commonly used citrus rootstock in Europe. Entomol Gen 40:79–86. https://doi.org/10.1127/entomologia/2020/0826

Wei ZH, Wang XQ, Li PR, Tan X, Yang X (2020) Diet-mediated effects of cadmium on the fitness-related traits and detoxification and antioxidative enzymes in the oriental armyworm, mythimna separata. Entomol Gen 40:407–419. https://doi.org/10.1127/entomologia/2020/0869

Werner BJ, Mowry TM, Bosque-Pérez NA, Ding HJ, Eigenbrode SD (2009) Changes in green peach aphid responses to Potato leafroll virus–induced volatiles emitted during disease progression. Environ Entomol 38:1429–1438. https://doi.org/10.1603/022.038.0511

Wu Y, Davis TS, Eigenbrode SD (2014) Aphid behavioral responses to virus-infected plants are similar despite divergent fitness effects. Entomol Exp Appl 153:246–255. https://doi.org/10.1111/eea.12246

Yang DS, Lee KS, Jeong OY, Kim KJ, Kays SJ (2008) Characterization of volatile aroma compounds in cooked black rice. J Agric Food Chem 56:235–240. https://doi.org/10.1021/jf072360c

Zhu JW, Park KC (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator coccinella septempunctata. J Chem Ecol 31(8):1733–1746. https://doi.org/10.1007/s10886-005-5923-8