Effect of soybean variety and systemic induction on herbivore feeding guilds

Abstract

Plants are attacked by a variety of herbivores and respond with localized or systemic defenses. Plant defense against one feeding guild (e.g. chewing, piercing/sucking) may also affect alternate feeding guilds. To optimize host plant resistance, interactions between feeding guilds must be understood. Aphids are plant virus vectors whose vector efficiency can be altered by plant defenses. To determine if systemic induction influences aphid feeding behaviors related to virus transmission, three soybean varieties, Davis, Lyon, and Progeny 4906RR, were induced by subjecting plants to soybean looper (SBL) herbivory, or exogenous applications of either jasmonic acid (JA) or salicylic acid (SA). Green peach aphid (GPA) apterae feeding behavior was recorded on induced and control plants using the Electrical Penetration Graph (EPG) technique. SBL growth bioassays were used to assess systemic induction. Previous SBL herbivory reduced SBL larval weights when fed Progeny 4906RR. JA reduced larval weights on Progeny 4906RR and Davis. SA increased SBL larval weights on Lyon. SBL herbivory decreased behaviors associated with nonpersistent virus transmission in Davis and Progeny 4906RR. JA altered behaviors associated with virus transmission in Davis and increased behaviors associated with virus acquisition in Progeny 4906RR. SA delayed probing in Davis, but increased behaviors associated with virus transmission in Progeny 4906RR and Lyon. Inducing host plant resistance with JA may reduce herbivore performance and increase nonpersistent virus transmission. Previous chewing herbivory may decrease nonpersistent virus transmission by aphids but is variety dependent.

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References

  1. Accamando AK, Cronin JT (2012) Costs and benefits of jasmonic acid induced responses in soybean. Environ Entomol 41:551–561

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  2. Anderson KE, Inouye BD, Underwood N (2015) Can inducible resistance in plants cause herbivore aggregations? Spatial patterns in an inducible plant/herbivore model. Ecology 96:2758–2770

    PubMed  Article  PubMed Central  Google Scholar 

  3. Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defenses. Biochem Biophys Acta 1734:91–111

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Baldwin IT (1999) Functional interactions in the use of direct and indirect defences in native Nicotiana plants. In: Chadwick J, Goode JA (eds) Insect-plant interactions and induced plant defense. Wiley, New York, pp 74–94

    Google Scholar 

  5. Boughton AJ, Hoover K, Felton GW (2006) Impact of chemical elicitor applications on greenhouse tomato plants and population growth of the green peach aphids, Myzus persicae. Entomol Exp Appl 120:175–188

    CAS  Article  Google Scholar 

  6. Cao H, Wang S, Liu T (2013) Jasmonate- and salicylate-induced defenses in wheat affect host preference and probing behavior, but not performance of the grain aphid Sitibion avenae. Insect Sci 00:1–9

    Google Scholar 

  7. Caviness CE, Walter HJ (1966) Registration of ‘Davis’ soybean. Crop Sci 6:502

    Article  Google Scholar 

  8. Chen M-S (2008) Inducible direct plant defenses against herbivores: a review. Insect Sci 15:101–114

    Article  CAS  Google Scholar 

  9. Collar JL, Fereres A (1998) Nonpersistent virus transmission efficiency determined by aphid probing behavior during intercellular punctures. Environ Entomol 27:583–591

    Article  Google Scholar 

  10. Collar JL, Avilla C, Fereres A (1997) New correlations between aphid stylet paths and nonpersistent virus transmission. Environ Entomol 26:537–544

    Article  Google Scholar 

  11. Coppola V, Soler R, Rao R, Corrado G (2017) Tomato-mediated interactions between root herbivores and aphids: insights into plant defense signaling. Entomol Exp Appl 163:170–176

    CAS  Article  Google Scholar 

  12. Davis JA, Radcliffe EB (2008) Reproduction and feeding behavior of Myzus persicae on four cereals. J Econ Entomol 101:9–16

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  13. Ellis C, Karafyllidis I, Turner JG (2002) Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol Plant Microbe Interact 15:1025–1030

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  14. Fehr WR, Caviness CE (1977) Stages of soybean development. Special report 87. http://lib.dr.iastate.edu/specialreports/87

  15. Felton GW, Eichenseer H (1999) Herbivore saliva and its effect on plant defence against herbivores and pathogens. In: Agrawal A, Tuzun S, Bent E (eds) Induced plant defenses against pathogens and herbivores. The American Phytopathological Society Press, St. Paul, pp 19–36

    Google Scholar 

  16. Felton GW, Summers CB, Muwller AJ (1994) Oxidative response in soybean foliage to herbivory by bean leaf beetle and three-cornered alfalfa hopper. J Chem Ecol 20:639–650

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  17. Fereres A, Moreno A (2009) Behavioral aspects influencing plant virus transmission by homopteran insects. Virus Res 141:158–168

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  18. Ferry N, Edwards MG, Gatehouse JA, Gatehouse AMR (2004) Plant-insect interactions: molecular approaches to insect resistance. Curr Opin Biotechnol 15:155–161

    CAS  PubMed  Article  Google Scholar 

  19. Gordy JW (2013) A survey of chemical elicitors and their effectiveness as promoters of plant defense against herbivory by Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) M.S. thesis, Louisiana State University

  20. Hartwig EE, Kilen TC, Young LD (1994) Registration of ‘Lyon’ soybean. Crop Sci 34:1412

    Article  Google Scholar 

  21. Hatchett JH, Beland GH, Hartwig EE (1976) Leaf-feeding resistance to bollworm and tobacco budworm in three soybean plant introductions. Crop Sci 16(2):277–280

    Article  Google Scholar 

  22. Heidel AJ, Baldwin IT (2004) Microarray analysis of salicylic acid- and jasmonic acid-signaling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds. Plant Cell Environ 27:1362–2137

    CAS  Article  Google Scholar 

  23. Heil M, Bueno JCS (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci 104:5467–5472

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  24. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  25. Kant MR, Jonckheere W, Knegt B et al (2015) Mechanisms and ecological consequences of plant defense induction and suppression in herbivore communities. Ann Bot 115:1015–1051

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. Katis NI, Tsitsipis JA, Stevens M, Powell G (2007) Transmission of plant viruses. In: Van Emden HF, Harrington R (eds) Aphids as crop pests, 1st edn. CABI, Wallingford, pp 87–113

    Google Scholar 

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  28. Michaud JP, Zhang Y, Bain C (2017) Feeding by Melanaphis sacchari (Hemiptera:Aphididae) facilitates use of sorghum by Rhopalisiphum padi (Hemiptera:Aphididae), but reciprocal effects are negative. Environ Entomol 42:268–273

    Google Scholar 

  29. Mitchell C, Breenan RM, Graham J, Karley AJ (2016) plant defense against herbivorous pests: exploiting resistance and tolerance traits for sustainable crop production. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01132/full

    Article  PubMed  PubMed Central  Google Scholar 

  30. Montllor CB, Tjalling WF (1989) Stylet penetration by two aphid species on susceptible and resistant lettuce. Entomol Exp Appl 52:103–111

    Article  Google Scholar 

  31. Morell K, Kessler A (2017) Plant communication in a widespread goldenrod: keeping herbivores on the move. Funct Ecol 31:1049–1061

    Article  Google Scholar 

  32. Musser RO, Cipollini DF, Hum-Musser SM, Williams SA, Brown JK, Felton GW (2005) Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants. Arch Insect Biochem Physiol 58:128–137

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  33. Ng JCK, Perry KL (2004) Transmission of plant viruses by aphid vectors. Mol Plant Pathol 5:505–511

    PubMed  Article  PubMed Central  Google Scholar 

  34. Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  35. Pickett JA, Chamberlain K, Poppy GM, Woodcock CM (1999) Exploiting insect responses in identifying plant signals. In: Chadwick J, Goode JA (eds) Insect-plant interactions and induced plant defense. Wiley, New York, pp 253–265

    Google Scholar 

  36. Poehlman JM (1987) Breeding soybeans. In: Poehlman JM (ed) Breeding field crops, 3rd edn. Van Nostrand Reinhold, New York, pp 421–450

    Google Scholar 

  37. Powell G (2005) Intracellular salivation is the aphid activity associated with inoculation of non-persistently transmitted viruses. J Gen Virol 86:469–472

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  38. Powell G, Pirone T, Hardie J (1995) Aphid stylet activities during potyvirus acquisition from plants and an in vitro system that correlate with subsequent transmission. Eur J Plant Pathol 101:411–420

    Article  Google Scholar 

  39. Prado E, Tjallingii WF (1997) Effects of previous plant infestation on sieve element acceptance by two aphids. Entomol Exp Appl 82:189–200

    Article  Google Scholar 

  40. Selig P, Keough S, Nalam VJ, Nachappa P (2016) Jasmonate-dependent plant defenses mediate soybean thrips and soybean aphid performance on soybean. Arthropod Plant Interact 10:273–282

    Article  Google Scholar 

  41. Smith CM, Boyko EV (2006) The molecular basis of plant resistance and defense responses to aphid feeding: current status. Entomol Exp Appl 122:1–16

    Article  CAS  Google Scholar 

  42. Smith CM, Clement SL (2012) Molecular basis of plant resistance to arthropods. Annu Rev Entomol 57:309–328

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  43. Srinivas P, Danielson SD (2001) Effect of the chemical inducer ActigardTM in inducing resistance to bean leaf beetle, Cerotoma trifurcate (Forster) (Coleoptera: Chysomelidae), feeding in soybean. J Agric Urban Entomol 18:209–215

    Google Scholar 

  44. Stout M, Davis J (2009) Keys to the increased use of host plant resistance in integrated pest management. In: Peshin R, Dhawan AK (eds) Integrated pest management: innovation-development process. Springer, Berlin, pp 163–180

    Google Scholar 

  45. Stout MJ, Workman KV, Bostock RM, Duffey SS (1998) Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113:74–81

    Article  Google Scholar 

  46. Tan XL, Chen JL, Benelli G, Desneux N, Yang XQ, Liu TX, Ge F (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 8:1–11

    Google Scholar 

  47. Underwood NC (1998) The timing of induced resistance and induced susceptibility in the soybean-Mexican bean beetle system. Oecologia 114:376–381

    PubMed  Article  PubMed Central  Google Scholar 

  48. Underwood NC, Morris W, Gross K, Lockwood JR III (2000) Induced resistance to Mexican bean beetle in soybean: variation among genotype and lack of correlation with constitutive resistance. Oecologia 122:83–89

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  49. Underwood NC, Rausher M, Cook W (2002) Bioassay versus chemical assay: measuring the impact of induced and constitutive resistance on herbivores in the field. Oecologia 131:211–219

    PubMed  Article  PubMed Central  Google Scholar 

  50. Van der Does D, Leon-Reyes A, Koornneef A et al (2013) Salicylic acid suppressed jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25:744–761

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  51. Vos IA, Pieterse CMJ, van Wees SCM (2013) Costs and benefits of hormone-regulated plant defense. Plant Path 62:43–55

    Article  Google Scholar 

  52. Walker GP (2000) A beginner’s guide to electronic monitoring of homopteran feeding behavior. In: Walker GP, Backus EA (eds) Principles and applications of electronic monitoring and other techniques in the study of homopteran feeding behavior. Entomological Society of America, Lanham, pp 14–40

    Google Scholar 

  53. Wosula EN, Clark CA, Davis JA (2012) Effect of host plant, aphid species, and virus infection status on transmission of Sweetpotato feathery mottle virus. Plant Dis 96:1331–1336

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  54. Xuan C, Richter AR, Stout MJ, Davis JA (2018) Effects of induced plant resistance on soybean looper (Lepidoptera: Noctuidae) in soybean. Arthropod Plant Interact 13:543–551

    Article  CAS  Google Scholar 

  55. Zhang Y, Fan J, Francis F, Chen J (2017) Watery saliva secreted by the grain aphid Sitbion avenae stimulates aphid resistance in wheat. J Agric Food Chem 65:8798–8805

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  56. Züst T, Agrawal AA (2017) Trade-offs between plant growth and defense against insect herbivory: an emerging mechanical synthesis. Annu Rev Plant Biol 68:513–534

    PubMed  Article  CAS  PubMed Central  Google Scholar 

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Acknowledgements

This article was approved for publication by the Director of the Louisiana Agricultural Experiment Station as manuscript No. 2020-234-34838.

Funding

This project was partially funded by the Louisiana Soybean and Grain Research and Promotion Board and by the Louisiana Agricultural Experiment Station.

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J.L.D. and J.A.D. designed the study. J.L.D. performed the experiments and analyzed the data. J.L.D. and J.A.D. wrote the manuscript and all authors reviewed the manuscript.

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Correspondence to John L. Dryburgh.

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Dryburgh, J.L., Davis, J.A. Effect of soybean variety and systemic induction on herbivore feeding guilds. Arthropod-Plant Interactions (2021). https://doi.org/10.1007/s11829-021-09806-8

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Keywords

  • Induced resistance
  • Virus transmission
  • Crosstalk
  • Trophic interaction