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Jasmonate-dependent plant defenses mediate soybean thrips and soybean aphid performance on soybean

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Abstract

Insect herbivores from different feeding guilds induce different signaling pathways in plants. In this study, we examined the effects of salicylic acid (SA)- and jasmonic acid (JA)-mediated defenses on performance of insect herbivores from two different feeding guilds: cell-content feeders, soybean thrips and phloem feeders, soybean aphids. We used a combination of RT-qPCR analysis and elicitor-induced plant resistance to determine induction of SA and JA signaling pathways and the impact on herbivore performance. In the early interaction between the host plant and the two herbivores, SA and JA signaling seems to occur simultaneously. But overall, soybean thrips induced JA-related marker genes, whereas soybean aphids increased SA and ABA-related marker genes over a 24-h period. Populations of both soybean thrips and soybean aphids were reduced (47 and 25 %, respectively) in methyl jasmonate (MeJA)-pretreated soybean plants. SA treatment has no effect on either herbivore performance. A combination pretreatment of SA and MeJA did not impact soybean thrips population but reduced soybean aphid numbers which was comparable with MeJA treatment. Our data suggest that SA–JA antagonism could be responsible for the effect of hormone pretreatment on thrips performance, but not on aphid performance. By linking plant defense gene expression and elicitor-induced resistance, we were able to pinpoint the role for JA signaling pathway in resistance to two herbivores from different feeding guilds.

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References

  • Abe H, Ohnishi J, Narusaka M, Seo S, Narusaka Y, Tsuda S, Kobayashi M (2008) Function of jasmonate in response and tolerance of Arabidopsis to thrips feeding. Plant Cell Physiol 49:68–80

    Article  CAS  PubMed  Google Scholar 

  • Abe H et al (2009) Jasmonate-dependent plant defense restricts thrips performance and preference. BMC Plant Biol 9:97

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302

    Article  CAS  PubMed  Google Scholar 

  • Bansal R, Mittapelly P, Cassone BJ, Mamidala P, Redinbaugh MG, Michel A (2015) Recommended reference genes for quantitative PCR analysis in soybean have variable stabilities during diverse biotic stresses. PLoS One. doi:10.1371/journal.pone.0134890

    Google Scholar 

  • Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    Article  CAS  PubMed  Google Scholar 

  • Boughton AJ, Hoover K, Felton GW (2005) Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersicon esculentum. J Chem Ecol 31:2211–2216

    Article  CAS  PubMed  Google Scholar 

  • Broekgaarden C, Voorrips RE, Dicke M, Vosman B (2011) Transcriptional responses of Brassica nigra to feeding by specialist insects of different feeding guilds. Insect Sci 18:259–272. doi:10.1111/j.1744-7917.2010.01368.x

    Article  CAS  Google Scholar 

  • Cao HH, Wang SH, Liu TX (2014) Jasmonate- and salicylate-induced defenses in wheat affect host preference and probing behavior but not performance of the grain aphid, Sitobion avenae. Insect Sci 21:47–55

    Article  CAS  PubMed  Google Scholar 

  • Cooper WC, Jia L, Goggin FL (2004) Acquired and R-gene mediated resistance against the potato aphid in tomato. J Chem Ecol 30:2527–2542. doi:10.1007/s10886-004-7948-9

    Article  CAS  PubMed  Google Scholar 

  • Duffey S (1986) Plant glandular trichomes: their partial role in defence against insects. In: Juniper B, Southwood R (eds) Insects and the plant surface. Edward Arnold, London, pp 151–172

    Google Scholar 

  • El-Wakeil NE, Volkmar C, Sallam AA (2010) Jasmonic acid induces resistance to economically important insect pests in winter wheat. Pest Manag Sci 66:549–554

    Article  CAS  PubMed  Google Scholar 

  • Ford KA et al (2010) Neonicotinoid insecticides induce salicylate-associated plant defense responses. Proc Natl Acad Sci USA 107:17527–17532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Verrall SR, Hancock RD (2015) Systematic analysis of phloem-feeding insect-induced transcriptional reprogramming in Arabidopsis highlights common features and reveals distinct responses to specialist and generalist insects. J Exp Bot 66:495–512

    Article  CAS  PubMed  Google Scholar 

  • Harwood JD, Desneux N, Yoo HJS, Rowley DL, Greenstone MH, Obrycki JJ (2007) Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach. Mol Ecol 16:4390–4400

    Article  CAS  PubMed  Google Scholar 

  • Heidel-Fischer HM, Musser RO, Vogel H (2014) Plant transcriptomic responses to herbivory. Annu Plant Rev Insect Plant Interact 47:155–196. doi:10.1002/9781118829783.ch5

    Article  CAS  Google Scholar 

  • Hodgson E, McCornack B, Tilmon K, Knodel J (2012) Management recommendations for soybean aphid (Hemiptera: Aphididae) in the United States. J Integr Pest Manag 3:E1–E10

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Huckaba RM, Coble HD, Van Duyn JW (1988) Joint effects of acifluorfen applications and soybean thrips (Sericothrips variabilis) feeding on soybean (Glycine max). Weed Sci 36:667–670

    CAS  Google Scholar 

  • Irwin ME, Yeargan KV, Marston NL (1979) Spatial and seasonal patterns of phytophagous thrips in soybean fields with comments on sampling techniques. Environ Entomol 8:131–140

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Klein AT et al (2015) Investigation of the chemical interface in the soybean-aphid and rice-bacteria interactions using MALDI-mass spectrometry imaging. Anal Chem 87:5294–5301

  • Le DT, Aldrich DL, Valliyodan B, Watanabe Y, Ha CV, Nishiyama R et al (2012) Evaluation of candidate reference genes for normalization of quantitative RT-PCR in soybean tissues under various abiotic stress conditions. PLoS ONE 7:e46487

  • Li Y, Zou J, Li M, Bilgin DD, Vodkin LO, Hartman GL, Clough SJ (2008) Soybean defense responses to the soybean aphid. New Phytol 179:185–195

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCΤ method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Mason HS, DeWald DB, Mullet JE (1993) Identification of a methyl jasmonate-responsive domain in the soybean vspB promoter. Plant Cell 5:241–251

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signaling pathways modulate arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol 138:1149–1162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Momol M, Olson S, Funderburk J, Stavisky J, Marois J (2004) Integrated management of tomato spotted wilt on field-grown tomatoes. Plant Dis 88:882–890

    Article  CAS  Google Scholar 

  • Mueller AJ (1994) Soybean thrips. In: Higley LG, Boethel DJ (eds) Handbook of soybean pests. Entomological Society of America, Lanham, MD

    Google Scholar 

  • Nalam VJ et al (2015) Facilitation of Fusarium graminearum infection by 9-lipoxygenases in Arabidopsis and wheat. Mol Plant Microbe Interact 28:1142–1152

    Article  CAS  PubMed  Google Scholar 

  • Novotny V et al (2010) Guild-specific patterns of species richness and host specialization in plant–herbivore food webs from a tropical forest. J Anim Ecol 79:1193–1203

    Article  PubMed  Google Scholar 

  • Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    Article  CAS  PubMed  Google Scholar 

  • Prochaska TJ, Donze-Reiner T, Marchi-Werle L, Palmer NA, Hunt TE, Sarath G, Heng-Moss T (2015) Transcriptional responses of tolerant and susceptible soybeans to soybean aphid (Aphis glycines Matsumura) herbivory. Arthropod Plant Interact 9:347–359

    Article  Google Scholar 

  • Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56:375–399

    Article  CAS  PubMed  Google Scholar 

  • Reisig DD, Herbert DA, Malone S (2012) Impact of neonicotinoid seed treatments on thrips (Thysanoptera: Thripidae) and soybean yield in Virginia and North Carolina. J Econ Entomol 105:884–889

    Article  CAS  PubMed  Google Scholar 

  • Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343

    Article  CAS  PubMed  Google Scholar 

  • Schoonhoven LM, Loon JJA, Dicke M (2005) Insect-plant biology, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Stam JM, Kroes A, Li Y, Gols R, van Loon JJ, Poelman EH, Dicke M (2014) Plant interactions with multiple insect herbivores: from community to genes. Plant Biol 65:689

    Article  CAS  Google Scholar 

  • Studham ME, MacIntosh GC (2012) Phytohormone signaling pathway analysis method for comparing hormone responses in plant–pest interactions. BMC Res Notes 5:392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Studham ME, MacIntosh GC (2013) Multiple phytohormone signals control the transcriptional response to soybean aphid infestation in susceptible and resistant soybean plants. Mol Plant Microbe Interact 26:116–129

    Article  CAS  PubMed  Google Scholar 

  • Szczepaniec A, Raupp MJ, Parker RD, Kerns D, Eubanks MD (2013) Neonicotinoid insecticides alter induced defenses and increase susceptibility to spider mites in distantly related crop plants. PLoS One. doi:10.1371/journal.pone.0062620

    PubMed  PubMed Central  Google Scholar 

  • Tally A, Oostendorp M, Lawton K, Staub T, Bassy B (1999) Commercial development of elicitors of induced resistance to pathogens. In: Agarwal AA, Tuzun S, Bent E (eds) Induced plant defenses against pathogens and herbivores: biochemistry, ecology, and agriculture, APS Press, St. Paul, pp 357–369

  • Thaler JS, Stout MJ, Karban R, Duffey SS (2001) Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol Entomol 26:312–324

    Article  Google Scholar 

  • Thaler JS, Agrawal AA, Halitschke R (2010) Salicylate-mediated interactions between pathogens and herbivores. Ecology 91:1075–1082. doi:10.1890/08-2347.1

    Article  PubMed  Google Scholar 

  • Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270

    Article  CAS  PubMed  Google Scholar 

  • Thompson GA, Goggin FL (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J Exp Bot 57:755

    Article  CAS  PubMed  Google Scholar 

  • Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    CAS  PubMed  Google Scholar 

  • Ward EW, Cahill DM, Bhattacharyya MK (1989) Abscisic acid suppression of phenylalanine ammonia-lyase activity and mRNA, and resistance of soybeans to Phytophthora megasperma f. sp. glycinea. Plant Physiol 91:23–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Y et al (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1:639–647

    Article  CAS  PubMed  Google Scholar 

  • Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Tzanetakis IE (2013) Epidemiology of Soybean vein necrosis-associated virus. Phytopathology 103:966–971

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was funded by Grants from the Indiana Academy of Sciences and Indiana Soybean Alliance. We thank Jenna Davidson, Lee Danels and Dominic Snowball for their help with the insect performance assays. We would also like to thank two anonymous reviewers for their feedback that significantly improved the manuscript.

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Correspondence to Punya Nachappa.

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Supplementary Fig. 1

Expression of salicylate-responsive PR1 and jasmonate-responsive JAR1 in plants treated with SA or MeJA. Reverse transcriptase-PCR (RT-PCR) was performed on RNA extracted from leaves of soybean plants 24 h after they were treated with 0.1 or 0.5 mM salicylic acid and 0.5 or 1.5 mM MeJA. RNA was also collected from plants that were treated with water as a control (C). Each lane on the gel image represents pooled RNA extracted from leaf tissue collected from three individual plants. Expression of soybean FBOX gene provided the control for RT-PCR (JPEG 27 kb)

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Selig, P., Keough, S., Nalam, V.J. et al. Jasmonate-dependent plant defenses mediate soybean thrips and soybean aphid performance on soybean. Arthropod-Plant Interactions 10, 273–282 (2016). https://doi.org/10.1007/s11829-016-9437-9

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