Abstract
Plant pathogens can influence host characteristics such as volatile emissions, nutrient composition or plant color, modulating vector and non-vector insect dynamics in the ecosystem. While previous research has focused on insect attraction and dispersal to infected plants, little is known about mechanisms mediating these interactions. Here, we investigate the role of ethylene in green peach aphid (Myzus persicae) attraction to potyvirus-infected plants. In our experiments, we utilized two different potyviruses, Potato virus Y (PVY) and Turnip mosaic virus, in lab and field experiments. Consistent with previous studies, we show that greater numbers of aphids settle on potyvirus-infected plants in the lab and greater numbers of aphids are found in PVY-infected potato (Solanum tuberosum) fields compared to controls. In laboratory experiments, inhibition of ethylene signaling in plants either chemically or genetically prevented aphids from preferentially settling on potyvirus-infected plants. Virus spread was reduced in lab arenas by over 80% when ethylene signaling was inhibited chemically. Despite this, ethylene inhibition had no significant impact on virus spread in field mesocosms. Our results indicate that induction of ethylene signaling by potyviruses mediates aphid attraction to infected plants and virus spread; however, additional factors may contribute to plant–vector dynamics in complex communities. Specific components of ethylene signaling may be important targets for future management of vector-borne viruses and research on mechanisms mediating plant–vector–virus interactions.
Similar content being viewed by others
References
Aartsma Y, Bianchi FJJA, van der Werf W, Poelman EH, Dicke M (2017) Herbivore-induced plant volatiles and tritrophic interactions across spatial scales. New Phytol 216(4):1054–1063
Adachi S, Honma T, Yasaka R, Ohshima K, Tokuda M (2018) Effects of infection by Turnip mosaic virus on the population growth of generalist specialist aphid vectors on turnip plants. PLoS One 13(7):e0200784
Arimura G, Tashiro K, Kuhara S, Nishioka T, Ozawa R, Takabayashi J (2000) Gene responses in bean leaves induced by herbivory and by herbivore-induced volatiles. Biochem Biophys Res Commun 277(2):305–310
Bak A, Cheung AL, Yang C, Whitham SA, Casteel CL (2017) A viral protease relocalizes in the presence of the vector to promote vector performance. Nat Commun 8:14493
Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488
Brigneti G, Voinnet O, Li WX, Ji LH, Ding SW, Baulcombe DC (1998) Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 17:6739–6746
Casteel CL, Hansen AK, Walling LL, Paine TD (2012) Manipulation of plant defense responses by the tomato psyllid (Bactericerca cockerelli) and its associated endosymbiont Candidatus Liberibacter psyllaurous. PLoS One 7:e35191
Casteel CL, Yang C, Nuri AC, De Jong HN, Whitham SA, Jander G (2014) The NIa-Pro protein of Turnip mosaic virus improves growth reproduction of the aphid vector Myzus persicae (green peach aphid). Plant J 77:653–663
Casteel CL, De Alwis M, Bak A, Dong H, Whitham SA, Jander G (2015) Disruption of ethylene responses by Turnip mosaic virus mediates suppression of plant defense against the green peach aphid vector. Plant Physiol 169:209–218
Chisholm PJ, Sertsuvalkul N, Casteel CL, Crowder DW (2018) Reciprocal plant-mediated interactions between a virus and a non-vector. Ecology 99:2139–2144
Dong X (1998) Salicylic acid, jasmonic acid, ethylene and disease resistance in plants. Curr Opin Plant Biol 1:316–323
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 Biol Sci 269:455–460
Eigenbrode SD, Bosque-Pérez NA, Davis TS (2018) Insect-borne plant pathogens and their vectors: ecology evolution and complex interactions. Annu Rev Entomol 63:169–191
Elzinga DA, De Vos M, Jander G (2014) Suppression of plant defenses by a Myzus persicae (green peach aphid) salivary effector protein. Mol Plant Microbe Interact 27:747–756
Even-Chen Z, Mattoo AK, Goren R (1982) Inhibition of ethylene biosynthesis by aminoethoxyvinylglycine and by polyamines shunts label from 3,4-[14C]methionine into spermidine in aged orange peel discs. Plant Physiol 69:385–388
FAO (2016). http://www.faoorg/3/a-i5555epdf. Accessed Nov 2018
Fereres A, Perez P, Gemeno C, Ponz F (1993) Transmission of spanish pepper-PVY and potato-PVY isolates by aphid (Homoptera Aphididae) vectors—epidemiologic implications. Environ Entomol 22:1260–1265
Fernandez-Conradi P, Jactel H, Robin C, Tack AJM, Castagneyrol B (2017) Fungi reduce preference and performance of insect herbivores on challenged plants. Ecology 99:300–311
Gray S, De Boer S, Lorenzen J, Karasev A, Whitworth J, Nolte P, Singh R, Boucher A, Xu H (2010) Potato virus Y: an evolving concern for potato crops in the United States and Canada. Plant Dis 94:1384–1397
Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523
Hogenhout SA, Ammar E-D, Whitfield AE, Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359
Horiuchi J, Arimura G, Ozawa R, Shimoda T, Takabayashi J, Nishioka T (2001) Exogenous ACC enhances volatiles production mediated by jasmonic acid in lima bean leaves. FEBS Lett 509:332–336
Hu Y, You J, Li C, Williamson VM, Wang C (2017) Ethylene response pathway modulates attractiveness of plant roots to soybean cyst nematode Heterodera glycines. Sci Rep 7:41282
Ingwell LL, Eigenbrode SD, Bosque-Perez NA (2012) Plant viruses alter insect behavior to enhance their spread. Sci Rep 2:578
Jiang W, Sheng Q, Zhou X-J, Zhang M-J, Liu X-J (2002) Regulation of detached corier leaf senescence by 1-methylcyclopropene ethylene. Postharvest Biol Technol 26:339–345
Johnson SN, Douglas AE, Woodward S, Hartley SE (2003) Microbial impacts on plant–herbivore interactions: the indirect effects of a birch pathogen on a birch aphid. Oecologia 134:388–396
Karasev AV, Gray SM (2013) Continuous emerging challenges of Potato virus Y in potato. Annu Rev Phytopathol 51:571–586
Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229
Kersch-Becker MF, Thaler JS (2013) Virus strains differentially induce plant susceptibility to aphid vectors and chewing herbivores. Oecologia 174:883–892
Khan I, Zada H, Said K, Khalil S, Ahmed Naeem M (2004) Modeling population dynamics of potato aphids in Swat. Pak Entomol 26:1–4
Kim SH, Lim SR, Hong SJ, Cho BK, Lee H, Lee CG, Choi HK (2016) Effect of ethephon as an ethylene-releasing compound on the metabolic profile of Chlorella vulgaris. J Agric Food Chem 64:4807–4816
Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2006) ETR1-JAR1-PAD2-dependent signaling pathways are involved in C6-aldehyde-induced defense responses of Arabidopsis. Plant Sci 171:415–423
Kriz JC, Danielson SD, Brle JR, Blankenship EE, Henebry GM (2006) Effects of aphid (Homoptera) abundance and surrounding vegetation on the encounter rate of Coccinellidae (Coleoptera), Chrysopidae (Neuroptera) and Nabidae (Hemiptera) in Alfalfa. J Entomol Sci 41:211–220
Lau JA, Lennon JT (2011) Evolutionary ecology of plant–microbe interactions: soil microbial structure alters selection on plant traits. New Phytol 192:215–224
Lewsey MG, Murphy AM, MacLean D, Dalchau N, Westwood JH, Macaulay K, Bennett MH, Moulin M, Hanke DE, Powell G, Smith AG, Carr JP (2010) Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol Plant Microbe Interact 23(7):835–845
Liu H, Wang Y, Xu J, Su T, Liu G, Ren D (2008) Ethylene signaling is required for the acceleration of cell death induced by the activation of AtMEK5 in Arabidopsis. Cell Res 18:422
Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162
Lu BB, Li XJ, Sun WW, Li L, Gao R, Zhu Q, Tian SM, Fu MQ, Yu HL, Tang XM, Zhang CL, Dong HS (2013) AtMYB44 regulates resistance to the green peach aphid and diamondback moth by activating EIN2-affected defences in Arabidopsis. Plant Biol 15:841–850
Lund ST, Stall RE, Klee HJ (1998) Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 10:371–382
Mantelin S, Bhattarai KK, Kaloshian I (2009) Ethylene contributes to potato aphid susceptibility in a compatible tomato host. New Phytol 183:444–456
Mauck KE, De Moraes CM, Mescher MC (2010) Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proc Natl Acad Sci USA 107:3600–3605
Ngumbi E, Eigenbrode SD, Bosque-Perez 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
Oerke EC (2006) Crop losses to pests. J Agric Sci 144:31–43
Perilla-Henao LM, Casteel CL (2016) Vector-borne bacterial plant pathogens: interactions with hemipteran insects and plants. Front Plant Sci 7:1163
Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: behavioral evolutionary applied perspectives. Annu Rev Entomol 51:309–330
Prado E, Tjallingii WF (2007) Behavioral evidence for local reduction of aphid-induced resistance. J Insect Sci 7:1–8
Ruther J, Kleier S (2005) Plant–plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. J Chem Ecol 31:2217–2222
Salvaudon L, Shykoff JA (2013) Variation in Arabidopsis developmental responses to oomycete infection: resillience vs changes in life history traits. New Phytol 197:919–926
Salvaudon L, De Moraes CM, Mescher MC (2013) Outcomes of co-infection by two potyviruses: implications for the evolution of manipulative strategies. Proc R Soc Lond B Biol Sci 280:1756
Samsatly J, Jawhari M, Najjar C, Sobh H, Abou-Jawdah Y (2014) Modification of serological techniques and their evaluation for detection of potato viruses in seed certification related activities. Crop Prot 61:51–57
Scala A, Allmann S, Mirabella R, Haring MA, Schuurink RC (2013) Green leaf volatiles: a plant’s multifunctional weapon against herbivores and pathogens. Int J Mol Sci 14:17781–17811
Schaller GE, Binder BM (2017) Inhibitors of ethylene biosynthesis signaling. Methods Mol Biol 1573:223–235
Schoonhoven LM, Van Loon B, van Loon JJA, Dicke M (2005) Insect–plant biology. Oxford University Press, Oxford (on demand)
Selig P, Keough S, Nalam VJ, Nachappa P (2016) Jasmonate-dependent plant defenses mechanisms mediate soybean thrips and soybean aphid performance on soybean. Arthropod Plant Interact 10:273–282
Senanayake DG, Holiday NJ (1988) Comparison of visual, sweep-net and whole plant bag sampling methods for estimating insect pest populations on potato. J Econ Entomol 81:1113–1119
Shikano I, Rosa C, Tan C-W, Felton GW (2017) Tritrophic interactions: microbe-mediated plant effects on insect herbivores. Annu Rev Phytopathol 55:313–333
Srinivasan R, Alvarez JM (2007) Effect of mixed viral infections (Potato virus Y-Potato leafroll virus) on biology preference of vectors Myzus persicae and Macrosiphum euphorbiae (Hemiptera: Aphididae). J Econ Entomol 100:646–655
Sum MSH, Yee SF, Eng L, Poili E, Lamdin J (2017) Development of an indirect ELISA and dot-blot assay for serological detection of Rice tungro disease. Biomed Res Int 2:1–7
Tack AJ, Dicke M (2013) Plant pathogens structure arthropod communities across multiple spatial and temporal scales. Funct Ecol 27:633–645
Thaler JS, Stout MJ, Karban R, Duffey SS (1996) Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J Chem Ecol 22:1767–1781
Tungadi T, Groen SC, Murphy AM, Pate AE, Iqbal J, Bruce TJA, Cunniffe NJ, Carr JP (2017) Cucumber mosaic virus and its 2b protein alter emission of host volatile organic compounds but not aphid vector settling in tobacco. Virol J 14:91
Turlings TCJ, Erb M (2018) Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu Rev Entomol 63(1):433–452
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wimken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72
van Loon LC, Geraats BPJ, Linthorst HJM (2006) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11:184–191
von Dahl CC, Baldwin IT (2007) Deciphering the role of ethylene in plant–herbivore interactions. J Plant Growth Regul 26:201–209
Wagner MR, Lundberg DS, Coleman-Derr D, Tringe SG, Tringe Dangl JL, Mitchell-Olds T (2014) Natural soil microbes alter flowering phenology and the intensity of selection on flowering times in a wild Arabidopsis relative. Ecol Lett 17:717–726
Wang Q, Li J, Dang C, Chang X, Fang Q, Stanley D, Ye G (2018) Rice dwarf virus infection alters green rice leafhopper host preference and feeding behavior. PLoS One 13(9):e0203364
Watkins CB (2006) The use of 1-methylcyclopropene (1-MCP) on fruits vegetables. Biotechnol Adv 24:389–409
Werner BJ, Mowry TM, Bosque-Perez NA, Ding H, Eigenbrode SD (2009) Changes in green peach aphid responses to Potato leafroll virus-induced volatiles emitted during disease progression. Environ Entomol 38:1429–1438
Whitfield AE, Falk BW, Rotenberg D (2015) Insect vector-mediated transmission of plant viruses. Virology 479–480:278–289
Yang YX, Ahammed GJ, Wu C, Fan SY, Zhou YH (2015) Crosstalk among jasmonate, salicylate and ethylene signaling pathways in plant disease immune responses. Curr Protein Pept Sci 16:450–461
Zhao S, Hong W, Wu J, Wang Y, Ji S, Zhu S, Wei C, Zhang J, Li Y (2017) A viral protein promotes host SAMS1 activity ethylene production for the benefit of virus infection. eLife. https://doi.org/10.7554/eLife.27529
Zhou H, Chen L, Liu Y, Chen J, Francis F (2016) Use of slow-release plant infochemicals to control aphids: a first investigation in a Belgian wheat field. Sci Rep 6:31552
Zhu L, Li Y, Li L, Yang J, Zhang M (2011) Ethylene is involved in leafy mustard systemic resistance to Turnip mosaic virus infection through the mitochondrial alternative oxidase pathway. Physiol Mol Plant Pathol 76:166–172
Zhu L, Guo J, Ma Z, Wang J, Zhou C (2018) Arabidopsis transcription factor MYB102 increases plant susceptibility to aphids by substantial activation of ethylene biosynthesis. Biomolecules 8:2
Ziebell H, Murphy AM, Groen SC, Tungadi T, Westwood JH, Lewsey MG, Moulin M, Kleczkowski A, Smith AG, Stevens M, Powell G, Carr JP (2011) Cucumber mosaic virus and its 2b RNA silencing suppressor modify plant–aphid interactions in tobacco. Sci Rep 1:187
Acknowledgements
We thank Lee Ann Richmond for valuable advice on ethylene measurements and use of a gas chromatograph. We thank Brian Pellissier for his help with the field trials. This publication was supported by the California Potato Research Advisory Board, an USDA-NIFA Agriculture and Food Research Initiative Award, 2013-2013-03265, a National Science Foundation award, PGRP-1723926 and University of California start-up funds to CLC.
Author information
Authors and Affiliations
Contributions
CLC conceived ideas and project, CLC and AB designed the experiments. AB, MFP, and LMPH performed the experiments. AB analyzed the data. CLC and AB wrote the manuscript with editorial advice from all other authors.
Corresponding author
Additional information
Communicated by Merijn Kant.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bak, A., Patton, M.F., Perilla-Henao, L.M. et al. Ethylene signaling mediates potyvirus spread by aphid vectors. Oecologia 190, 139–148 (2019). https://doi.org/10.1007/s00442-019-04405-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-019-04405-0