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Mechanisms and evolution of plant resistance to aphids

Nature Plants volume 2, Article number: 15206 (2016) Cite this article

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Abstract

Aphids are important herbivores of both wild and cultivated plants. Plants rely on unique mechanisms of recognition, signalling and defence to cope with the specialized mode of phloem feeding by aphids. Aspects of the molecular mechanisms underlying aphid–plant interactions are beginning to be understood. Recent advances include the identification of aphid salivary proteins involved in host plant manipulation, and plant receptors involved in aphid recognition. However, a complete picture of aphid–plant interactions requires consideration of the ecological outcome of these mechanisms in nature, and the evolutionary processes that shaped them. Here we identify general patterns of resistance, with a special focus on recognition, phytohormonal signalling, secondary metabolites and induction of plant resistance. We discuss how host specialization can enable aphids to co-opt both the phytohormonal responses and defensive compounds of plants for their own benefit at a local scale. In response, systemically induced resistance in plants is common and often involves targeted responses to specific aphid species or even genotypes. As co-evolutionary adaptation between plants and aphids is ongoing, the stealthy nature of aphid feeding makes both the mechanisms and outcomes of these interactions highly distinct from those of other herbivore–plant interactions.

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Figure 1: A schematic of cardenolide sequestration and exudation by four aphid species on common milkweed (Asclepias syriaca, middle).

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References

  1. Blackman, R. L. & Eastop, V. F. Aphids on the World's Crops: an Identification and Information Guide (Wiley, 2000).

    Google Scholar 

  2. Douglas, A. E. The nutritional quality of phloem sap utilized by natural aphid populations. Ecol. Entomol. 18, 31–38 (1993).

    Article  Google Scholar 

  3. Dixon, A. F. G. Aphid Ecology 2nd edn (Chapman & Hall, 1998).

    Google Scholar 

  4. Douglas, A. E. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43, 17–37 (1998).

    Article  CAS  PubMed  Google Scholar 

  5. Agrawal, A. A. Induced responses to herbivory and increased plant performance. Science 279, 1201–1202 (1998).

    Article  CAS  PubMed  Google Scholar 

  6. Züst, T. et al. Natural enemies drive geographic variation in plant defenses. Science 338, 116–119 (2012).

    Article  PubMed  CAS  Google Scholar 

  7. Lankau, R. A. Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytol. 175, 176–184 (2007).

    Article  PubMed  Google Scholar 

  8. Elzinga, D. A. & Jander, G. The role of protein effectors in plant-aphid interactions. Curr. Opin. Plant Biol. 16, 451–456 (2013).

    Article  CAS  PubMed  Google Scholar 

  9. Ng, J. C. K. & Perry, K. L. Transmission of plant viruses by aphid vectors. Mol. Plant Pathol. 5, 505–511 (2004).

    Article  PubMed  Google Scholar 

  10. Powell, G., Tosh, C. R. & Hardie, J. Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Annu. Rev. Entomol. 51, 309–330 (2006).

    Article  CAS  PubMed  Google Scholar 

  11. Will, T., Furch, A. C. U. & Zimmermann, M. R. How phloem-feeding insects face the challenge of phloem-located defenses. Front. Plant Sci. 4, 336 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Walling, L. L. Avoiding effective defenses: Strategies employed by phloem-feeding insects. Plant Physiol. 146, 859–866 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Tjallingii, W. F. Salivary secretions by aphids interacting with proteins of phloem wound responses. J. Exp. Bot. 57, 739–745 (2006).

    Article  CAS  PubMed  Google Scholar 

  14. Kaloshian, I. Gene-for-gene disease resistance: bridging insect pest and pathogen defense. J. Chem. Ecol. 30, 2419–2438 (2004).

    Article  CAS  PubMed  Google Scholar 

  15. Prince, D. C., Drurey, C., Zipfel, C. & Hogenhout, S. A. The leucine-rich repeat receptor-like kinase BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 and the cytochrome P450 PHYTOALEXIN DEFICIENT3 contribute to innate immunity to aphids in Arabidopsis. Plant Physiol. 164, 2207–2219 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Smith, C. M. & Clement, S. L. Molecular bases of plant resistance to arthropods. Annu. Rev. Entomol. 57, 309–328 (2012).

    Article  CAS  PubMed  Google Scholar 

  17. Walling, L. L. in Advances in Botanical Research: Plant Innate Immunity Vol. 51 (ed. van Loon, L. C. ) 551–612 (2009).

    Google Scholar 

  18. Jaouannet, M. et al. Plant immunity in plant–aphid interactions. Front. Plant Sci. 5, 663 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Goggin, F. L. Plant–aphid interactions: molecular and ecological perspectives. Curr. Opin. Plant Biol. 10, 399–408 (2007).

    Article  CAS  PubMed  Google Scholar 

  20. Kessler, A. & Baldwin, I. T. Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53, 299–328 (2002).

    Article  CAS  PubMed  Google Scholar 

  21. Gao, L.-L. et al. Involvement of the octadecanoid pathway in bluegreen aphid resistance in Medicago truncatula. Mol. Plant Microbe Interact. 20, 82–93 (2007).

    Article  CAS  PubMed  Google Scholar 

  22. Walling, L. L. The myriad plant responses to herbivores. J. Plant Growth Regul. 19, 195–216 (2000).

    CAS  PubMed  Google Scholar 

  23. Cooper, W. C., Jia, L. & Goggin, F. L. Acquired and R-gene-mediated resistance against the potato aphid in tomato. J. Chem. Ecol. 30, 2527–2542 (2004).

    Article  CAS  PubMed  Google Scholar 

  24. Ali, J. G. & Agrawal, A. A. Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds. Func. Ecol. 28, 1404–1412 (2014).

    Article  Google Scholar 

  25. Stout, M. J., Workman, K. V., Bostock, R. M. & Duffey, S. S. Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113, 74–81 (1998).

    Article  Google Scholar 

  26. Ajlan, A. M. & Potter, D. A. Lack of effect of tobacco mosaic virus-induced systemic acquired resistance on arthropod herbivores in tobacco. Phytopathology 82, 647–651 (1992).

    Article  Google Scholar 

  27. Moran, P. J. & Thompson, G. A. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol. 125, 1074–1085 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Thaler, J. S., Agrawal, A. A. & Halitschke, R. Salicylate-mediated interactions between pathogens and herbivores. Ecology 91, 1075–1082 (2010).

    Article  PubMed  Google Scholar 

  29. Thaler, J. S., Humphrey, P. T. & Whiteman, N. K. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci. 17, 260–270 (2012).

    Article  CAS  PubMed  Google Scholar 

  30. Mewis, I., Appel, H. M., Hom, A., Raina, R. & Schultz, J. C. Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol. 138, 1149–1162 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ferry, N. et al. Molecular interactions between wheat and cereal aphid (Sitobion avenae): analysis of changes to the wheat proteome. Proteomics 11, 1985–2002 (2011).

    Article  CAS  PubMed  Google Scholar 

  32. Molyneux, R. J., Campbell, B. C. & Dreyer, D. L. Honeydew analysis for detecting phloem transport of plant natural products — implications for host-plant resistance to sap-sucking insects. J. Chem. Ecol. 16, 1899–1909 (1990).

    Article  CAS  PubMed  Google Scholar 

  33. Roberts, M. F. & Wink, M. Alkaloids: Biochemistry, Ecology, and Medicinal Applications (Plenum, 1998).

    Book  Google Scholar 

  34. Agrawal, A. A., Petschenka, G., Bingham, R. A., Weber, M. G. & Rasmann, S. Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol. 194, 28–45 (2012).

    Article  CAS  PubMed  Google Scholar 

  35. Botha, C. E. J., Malcolm, S. B. & Evert, R. F. An investigation of preferential feeding habit in four Asclepiadaceae by the aphid Aphis nerii B. de F. Protoplasma 92, 1–19 (1977).

    Article  Google Scholar 

  36. Züst, T. & Agrawal, A. A. Population growth and sequestration of plant toxins along a gradient of specialization in four aphid species on the common milkweed Asclepias syriaca. Func. Ecol. http://dx.doi.org/10.1111/1365-2435.12523 (2015).

  37. Agrawal, A. A. Plant defense and density dependence in the population growth of herbivores. Am. Nat. 164, 113–120 (2004).

    Article  PubMed  Google Scholar 

  38. Desneux, N., Barta, R. J., Hoelmer, K. A., Hopper, K. R. & Heimpel, G. E. Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 160, 387–398 (2009).

    Article  PubMed  Google Scholar 

  39. Blackman, R. L. & Eastop, V. F. Aphids on the World's Herbaceous Plants and Shrubs (Wiley, 2006).

    Google Scholar 

  40. Dreyer, D. L., Jones, K. C. & Molyneux, R. J. Feeding deterrency of some pyrrolizidine, indolizidine, and quinolizidine alkaloids towards pea aphid (Acyrthosiphon pisum) and evidence for phloem transport of indolizidine alkaloid swainsonine. J. Chem. Ecol. 11, 1045–1051 (1985).

    Article  CAS  PubMed  Google Scholar 

  41. Gü ntner, C. et al. Effect of Solanum glycoalkaloids on potato aphid, Macrosiphum euphorbiae. J. Chem. Ecol. 23, 1651–1659 (1997).

    Article  Google Scholar 

  42. Wink, M. & Witte, L. Storage of quinolizidine alkaloids in Macrosiphum albifrons and Aphis genistae (Homoptera: Aphididiae). Entomol. Gen. 15, 237–254 (1991).

    Article  Google Scholar 

  43. Witte, L., Ehmke, A. & Hartmann, T. Interspecific flow of pyrrolizidine alkaloids: from plants via aphids to ladybirds. Naturwissenschaften 77, 540–543 (1990).

    Article  CAS  Google Scholar 

  44. Wink, M., Hartmann, T., Witte, L. & Rheinheimer, J. Interrelationship between quinolizidine alkaloid-producing legumes and infesting insects: exploitation of the alkaloid-containing phloem sap of Cytisus scoparius by the broom aphid Aphis cytisorum. Z. Naturforsch. C 37, 1081–1086 (1982).

    Article  Google Scholar 

  45. Wink, M. & Römer, P. Acquired toxicity - the advantages of specializing on alkaloid-rich lupins to Macrosiphon albifrons (Aphidae). Naturwissenschaften 73, 210–212 (1986).

    Article  CAS  Google Scholar 

  46. Zuniga, G. E., Argandona, V. H., Niemeyer, H. M. & Corcuera, L. J. Hydroxamic acid content in wild and cultivated graminae. Phytochemistry 22, 2665–2668 (1983).

    Article  CAS  Google Scholar 

  47. Meihls, L. N. et al. Natural variation in maize aphid resistance is associated with 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside methyltransferase activity. Plant Cell 25, 2341–2355 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Grambow, H. J., Lückge, J., Klausener, A. & Müller, E. Occurrence of 2-(2-hydroxy-4,7-dimethoxy-2h-1,4-benzoxazin-3-one)-beta-d-glucopyranoside in Triticum aestivum leaves and its conversion into 6-methoxy-benzoxazolinone. Z. Naturforsch. C 41, 684–690 (1986).

    Article  CAS  Google Scholar 

  49. Ahmad, S. et al. Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiol. 157, 317–327 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Kim, J. H. & Jander, G. Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J. 49, 1008–1019 (2007).

    Article  CAS  PubMed  Google Scholar 

  51. Kim, J. H., Lee, B. W., Schroeder, F. C. & Jander, G. Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant J. 54, 1015–1026 (2008).

    Article  CAS  PubMed  Google Scholar 

  52. Francis, F., Lognay, G., Wathelet, J. P. & Haubruge, E. Effects of allelochemicals from first (Brassicaceae) and second (Myzus persicae and Brevicoryne brassicae) trophic levels on Adalia bipunctata. J. Chem. Ecol. 27, 243–256 (2001).

    Article  CAS  PubMed  Google Scholar 

  53. Goodey, N. A., Florance, H. V., Smirnoff, N. & Hodgson, D. J. Aphids pick their poison: selective sequestration of plant chemicals affects host plant use in a specialist herbivore. J. Chem. Ecol. 41, 956–964 (2015).

    Article  CAS  PubMed  Google Scholar 

  54. Cole, R. A. The relative importance of glucosinolates and amino acids to the development of two aphid pests Brevicoryne brassicae and Myzus persicae on wild and cultivated brassica species. Entomol. Exp. Appl. 85, 121–133 (1997).

    Article  CAS  Google Scholar 

  55. Saheed, S. A. et al. Stronger induction of callose deposition in barley by Russian wheat aphid than bird cherry-oat aphid is not associated with differences in callose synthase or β-1,3-glucanase transcript abundance. Physiol. Plant. 135, 150–161 (2009).

    Article  CAS  PubMed  Google Scholar 

  56. Dogimont, C., Chovelon, V., Pauquet, J., Boualem, A. & Bendahmane, A. The Vat locus encodes for a CC-NBS-LRR protein that confers resistance to Aphis gossypii infestation and A. gossypii-mediated virus resistance. Plant J. 80, 993–1004 (2014).

    Article  CAS  PubMed  Google Scholar 

  57. Chaudhary, R., Atamian, H. S., Shen, Z., Brigg, S. P. & Kaloshian, I. GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense. Proc. Natl Acad. Sci. USA 111, 8919–8924 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Keith, R. & Mitchell-Olds, T. Genetic variation for resistance to herbivores and plant pathogens: hypotheses, mechanisms and evolutionary implications. Plant Path. 62, 122–132 (2013).

    Article  Google Scholar 

  59. Sauge, M.-H. et al. Genotypic variation in induced resistance and induced susceptibility in the peach - Myzus persicae aphid system. Oikos 113, 305–313 (2006).

    Article  Google Scholar 

  60. Li, Y., Hill, C. B., Carlson, S. R., Diers, B. W. & Hartman, G. L. Soybean aphid resistance genes in the soybean cultivars Dowling and Jackson map to linkage group M. Mol. Breed. 19, 25–34 (2007).

    Article  CAS  Google Scholar 

  61. Goggin, F. L., Williamson, V. M. & Ullman, D. E. Variability in the response of Macrosiphum euphorbiae and Myzus persicae (Hemiptera: Aphididae) to the tomato resistance gene Mi. Environ. Entomol. 30, 101–106 (2001).

    Article  Google Scholar 

  62. Thomas, S., Dogimont, C. & Boissot, N. Association between Aphis gossypii genotype and phenotype on melon accessions. Arthropod Plant Interact. 6, 93–101 (2012).

    Article  Google Scholar 

  63. Sauge, M. H., Lacroze, J. P., Poessel, J. L., Pascal, T. & Kervella, J. Induced resistance by Myzus persicae in the peach cultivar ‘Rubira’. Entomol. Exp. Appl. 102, 29–37 (2002).

    Article  Google Scholar 

  64. Li, Q., Xie, Q. G., Smith-Becker, J., Navarre, D. A. & Kaloshian, I. Mi-1- mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Mol. Plant Microbe Interact. 19, 655–664 (2006).

    Article  CAS  PubMed  Google Scholar 

  65. Dixon, A. F. G. Stabilization of aphid populations by an aphid induced plant factor. Nature 227, 1368–1369 (1970).

    Article  Google Scholar 

  66. Wool, D. & Hales, D. F. Previous infestation affects recolonization of cotton by Aphis gossypii: Induced resistance or plant damage? Phytoparasitica 24, 39–48 (1996).

    Article  Google Scholar 

  67. Prado, E. & Tjallingii, W. F. Behavioral evidence for local reduction of aphid-induced resistance. J. Insect Sci. 7,, 48 (2007).

  68. Dugravot, S. et al. Local and systemic responses induced by aphids in Solanum tuberosum plants. Entomol. Exp. Appl. 123, 271–277 (2007).

    Article  Google Scholar 

  69. Brunissen, L., Cherqui, A., Pelletier, Y., Vincent, C. & Giordanengo, P. Host-plant mediated interactions between two aphid species. Entomol. Exp. Appl. 132, 30–38 (2009).

    Article  Google Scholar 

  70. Gianoli, E. Competition in cereal aphids (Homoptera: Aphididae) on wheat plants. Environ. Entomol. 29, 213–219, (2000).

    Article  Google Scholar 

  71. Mehrparvar, M., Mansouri, S. M. & Weisser, W. W. Mechanisms of species-sorting: effect of habitat occupancy on aphids' host plant selection. Ecol. Entomol. 39, 281–289 (2014).

    Article  Google Scholar 

  72. Kidd, N. A. C., Lewis, G. B. & Howell, C. A. An association between two species of pine aphid, Schizolachnus pineti and Eulachnus agilis. Ecol. Entomol. 10, 427–432 (1985).

    Article  Google Scholar 

  73. Sandström, J., Telang, A. & Moran, N. A. Nutritional enhancement of host plants by aphids - a comparison of three aphid species on grasses. J. Insect Physiol. 46, 33–40 (2000).

    Article  PubMed  Google Scholar 

  74. Inbar, M., Eshel, A. & Wool, D. Interspecific competition among phloem-feeding insects mediated by induced host-plant sinks. Ecology 76, 1506–1515 (1995).

    Article  Google Scholar 

  75. Kaplan, I., Sardanelli, S., Rehill, B. J. & Denno, R. F. Toward a mechanistic understanding of competition in vascular-feeding herbivores: an empirical test of the sink competition hypothesis. Oecologia 166, 627–636 (2011).

    Article  PubMed  Google Scholar 

  76. Girousse, C., Moulia, B., Silk, W. & Bonnemain, J. L. Aphid infestation causes different changes in carbon and nitrogen allocation in Alfalfa stems as well as different inhibitions of longitudinal and radial expansion. Plant Physiol. 137, 1474–1484 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Petersen, M. K. & Sandströ m, J. P. Outcome of indirect competition between two aphid species mediated by responses in their common host plant. Func. Ecol. 15, 525–534 (2001).

    Article  Google Scholar 

  78. Ni, X. Z. & Quisenberry, S. S. Diuraphis noxia and Rhopalosiphum padi (Hemiptera: Aphididae) interactions and their injury on resistant and susceptible cereal seedlings. J. Econ. Entomol. 99, 551–558 (2006).

    Article  PubMed  Google Scholar 

  79. Petterson, J., Quiroz, A. & Fahad, A. E. Aphid antixenosis mediated by volatiles in cereals. Acta Agr. Scand. B 46, 135–140 (1996).

    Google Scholar 

  80. Babikova, Z. et al. Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol. Lett. 16, 835–843 (2013).

    Article  PubMed  CAS  Google Scholar 

  81. Dicke, M. Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomol. Exp. Appl. 91, 131–142 (1999).

    Article  CAS  Google Scholar 

  82. Du, Y. J., Poppy, G. M. & Powell, W. Relative importance of semiochemicals from first and second trophic levels in host foraging behavior of Aphidius ervi. J. Chem. Ecol. 22, 1591–1605 (1996).

    Article  CAS  PubMed  Google Scholar 

  83. Guerrieri, E., Poppy, G. M., Powell, W., Tremblay, E. & Pennacchio, F. Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi. J. Chem. Ecol. 25, 1247–1261 (1999).

    Article  CAS  Google Scholar 

  84. Petrescu, A. S., Mondor, E. B. & Roitberg, B. D. Subversion of alarm communication: Do plants habituate aphids to their own alarm signals? Can. J. Zool. 79, 737–740 (2001).

    Article  Google Scholar 

  85. Du, Y. J. et al. Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J. Chem. Ecol. 24, 1355–1368 (1998).

    Article  CAS  Google Scholar 

  86. Prado, E. & Tjallingii, W. F. Effects of previous plant infestation on sieve element acceptance by two aphids. Entomol. Exp. Appl. 82, 189–200 (1997).

    Article  Google Scholar 

  87. Cardoza, Y. J., Reidy-Crofts, J. & Edwards, O. R. Differential inter- and intra-specific defense induction in Lupinus by Myzus persicae feeding. Entomol. Exp. Appl. 117, 155–163 (2005).

    Article  Google Scholar 

  88. Gianoli, E. Within-plant distribution of Rhopalosiphum padi on wheat seedlings is affected by induced responses. Entomol. Exp. Appl. 93, 227–230 (1999).

    Article  Google Scholar 

  89. Messina, F. J., Taylor, R. & Karren, M. E. Divergent responses of two cereal aphids to previous infestation of their host plant. Entomol. Exp. Appl. 103, 43–50 (2002).

    Article  Google Scholar 

  90. Hansen, A. K. & Moran, N. A. The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol. Ecol. 23, 1473–1496 (2014).

    Article  PubMed  Google Scholar 

  91. Ward, S. A., Leather, S. R., Pickup, J. & Harrington, R. Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? J. Anim. Ecol. 67, 763–773 (1998).

    Article  Google Scholar 

  92. Döring, T. F. How aphids find their host plants, and how they don't. Ann. Appl. Biol. 165, 3–26 (2014).

    Article  Google Scholar 

  93. Smith, M. T. & Severson, R. F. Host recognition by the blackmargined aphid (Homoptera: Aphididae) on pecan. J. Entomol. Sci. 27, 93–112 (1992).

    Article  CAS  Google Scholar 

  94. Thurston, R., Smith, W. T. & Cooper, B. P. Alkaloid secretion by trichomes of Nicotiana species and resistance to aphids. Entomol. Exp. Appl. 9, 428–432 (1966).

    Article  CAS  Google Scholar 

  95. Miles, P. W. The saliva of Hemiptera. Adv. Insect Physiol. 9, 183–255 (1972).

    Article  CAS  Google Scholar 

  96. Hewer, A., Will, T. & van Bel, A. J. E. Plant cues for aphid navigation in vascular tissues. J. Exp. Biol. 213, 4030–4042 (2010).

    Article  PubMed  Google Scholar 

  97. Turley, N. E. & Johnson, M. T. J. Ecological effects of aphid abundance, genotypic variation, and contemporary evolution on plants. Oecologia, 1–13 (2015).

  98. Pilson, D. Aphid distribution and the evolution of goldenrod resistance. Evolution 46, 1358–1372 (1992).

    Article  PubMed  Google Scholar 

  99. Turcotte, M. M., Lochab, A. K., Turley, N. E. & Johnson, M. T. J. Plant domestication slows pest evolution. Ecol. Lett. 18, 907–915 (2015).

    Article  PubMed  Google Scholar 

  100. Fraser, L. H. & Grime, J. P. Aphid fitness on 13 grass species: a test of plant defence theory. Can. J. Bot. 77, 1783–1789 (1999).

    Article  Google Scholar 

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Acknowledgements

We thank Georg Jander (Boyce Thompson Institute for Plant Research), Susanne Dobler (University of Hamburg) and the Phytophagy Lab at Cornell University (www.herbivory.com) for comments on the manuscript. T.Z. is supported by SNSF grants PBZHP3-141434 and P300P3-151191, and A.A.A. is supported by NSF-DEB-1513839 and a grant from the Templeton Foundation.

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    Present address: †Present address: Institute of Plant Sciences, University of Bern, Bern, CH-3013, Switzerland.,

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  1. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, 14853, New York, USA

    Tobias Züst & Anurag A. Agrawal

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Züst, T., Agrawal, A. Mechanisms and evolution of plant resistance to aphids. Nature Plants 2, 15206 (2016). https://doi.org/10.1038/nplants.2015.206

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