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Adaptation to Nicotine Feeding in Myzus persicae

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Abstract

Lineages of the generalist hemipteran herbivore Myzus persicae (green peach aphid) that have expanded their host range to include tobacco often have elevated nicotine tolerance. The tobacco-adapted M. persicae lineage used in this study was able to reproduce on nicotine-containing artificial diets at concentrations that were 15-fold higher than those that were lethal to a non-adapted M. persicae lineage. Fecundity of the nicotine-tolerant M. persicae lineage was increased by 100 μM nicotine in artificial diet, suggesting that this otherwise toxic alkaloid can serve as a feeding stimulant at low concentrations. This lineage also was pre-adapted to growth on tobacco, exhibiting no drop in fecundity when it was moved onto tobacco from a different host plant. Although growth of the non-tobacco-adapted M. persicae lineage improved after three generations on tobacco, this higher reproductive rate was not associated with increased nicotine tolerance. Myzus persicae gene expression microarrays were used to identify transcripts that are up-regulated in response to nicotine in the tobacco-adapted lineage. Induced expression was found for CYP6CY3, which detoxifies nicotine in M. persicae, other genes encoding known classes of detoxifying enzymes, and genes encoding secreted M. persicae salivary proteins.

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References

  • Bass C, Zimmer CT, Riveron JM, Wilding CS, Wondji CS, Kaussmann M, Field LM, Williamson MS, Nauen R (2014) Gene amplification and microsatellite polymorphism underlie a recent insect host shift. Proc Natl Acad Sci U S A 110:19460–19465

    Article  Google Scholar 

  • Blackman RL, Eastop VF (2000) Aphids on the world’s crops. Wiley, Chichester

    Google Scholar 

  • Brennan Y, Callen WN, Christoffersen L, Dupree P, Goubet F, Healey S, Hernandez M, Keller M, Li K, Palackal N et al (2004) Unusual microbial xylanases from insect guts. Appl Environ Microbiol 70:3609–3617

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cardoza YJ, Wang SF, Reidy-Crofts J, Edwards OR (2006) Phloem alkaloid tolerance allows feeding on resistant Lupinus angustifolius by the aphid Myzus persicae. J Chem Ecol 32:1965–1976

    Article  CAS  PubMed  Google Scholar 

  • Carolan JC, Fitzroy CI, Ashton PD, Douglas AE, Wilkinson TL (2009) The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 9:2457–2467

    Article  CAS  PubMed  Google Scholar 

  • Carolan JC, Caragea D, Reardon KT, Mutti NS, Dittmer N, Pappan K, Cui F, Castaneto M, Poulain J, Dossat C et al (2011) Predicted effector molecules in the salivary secretome of the pea aphid (Acyrthosiphon pisum): a dual transcriptomic/proteomic approach. J Proteome Res 10:1505–1518

    Article  CAS  PubMed  Google Scholar 

  • Cooper WR, Dillwith JW, Puterka GJ (2010) Salivary proteins of Russian wheat aphid (Hemiptera: Aphididae). Environ Entomol 39:223–231

    Article  CAS  PubMed  Google Scholar 

  • Cooper WR, Dillwith JW, Puterka GJ (2011) Comparisons of salivary proteins from five aphid (Hemiptera: Aphididae) species. Environ Entomol 40:151–156

    Article  CAS  PubMed  Google Scholar 

  • Cui F, Smith CM, Reese J, Edwards O, Reeck G (2012) Polymorphisms in salivary-gland transcripts of Russian wheat aphid biotypes 1 and 2. Insect Sci 19:429–440

    Article  CAS  Google Scholar 

  • Devine GJ, Harling ZK, Scarr AW, Devonshire AL (1996) Lethal and sublethal effects of imidacloprid on nicotine-tolerant Myzus nicotinianae and Myzus persicae. Pestic Sci 48:57–62

    Article  CAS  Google Scholar 

  • 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

  • Harmel N, Letocart E, Cherqui A, Giordanengo P, Mazzucchelli G, Guillonneau F, De Pauw E, Haubruge E, Francis F (2008) Identification of aphid salivary proteins: a proteomic investigation of Myzus persicae. Insect Mol Biol 17:165–174

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kinnersley AM, Dougall DK (1980) Correlation between the nicotine content of tobacco plants and callus cultures. Planta 149:205–206

    Article  CAS  PubMed  Google Scholar 

  • Kliot A, Kontsedalov S, Ramsey JS, Jander G, Ghanim M (2014) Adaptation to nicotine in the facultative tobacco-feeding hemipteran Bemisia tabaci. Pest Manag Sci. doi:10.1002/ps.3739

  • Kumar P, Pandit SS, Steppuhn A, Baldwin IT (2014) Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46’s role in a nicotine-mediated antipredator herbivore defense. Proc Natl Acad Sci U S A 111:1245–1252

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Leshkowitz D, Gazit S, Reuveni E, Ghanim M, Czosnek H, McKenzie C, Shatters RL Jr, Brown JK (2006) Whitefly (Bemisia tabaci) genome project: analysis of sequenced clones from egg, instar, and adult (viruliferous and non-viruliferous) cDNA libraries. BMC Genomics 7:79

    Article  PubMed Central  PubMed  Google Scholar 

  • Margaritopoulos JT, Kasprowicz L, Mallock GL, Fenton B (2009) Tracking the global dispersal of a cosmopolitan insect pest, the peach potato aphid. BMC Ecol 9:13

    Article  PubMed Central  PubMed  Google Scholar 

  • Miles PW (1999) Aphid Saliva. Biol Rev 74:41–85

    Article  Google Scholar 

  • Murray CL, Quaglia M, Arnason JT, Morris CE (1994) A putative nicotine pump at the metabolic blood-brain barrier of the tobacco hornworm. J Neurobiol 25:23–34

    Article  CAS  PubMed  Google Scholar 

  • Nauen R, Denholm I (2005) Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. Arch Insect Biochem Physiol 58:200–215

    Article  CAS  PubMed  Google Scholar 

  • Nicholson SJ, Hartson SD, Puterka GJ (2012) Proteomic analysis of secreted saliva from Russian wheat aphid (Diuraphis noxia Kurd.) biotypes that differ in virulence to wheat. J Proteome 75:2252–2268

    Article  CAS  Google Scholar 

  • Olivares-Donoso R, Troncoso AJ, Tapia DH, Aguilera-Olivares D, Niemeyer HM (2007) Contrasting performances of generalist and specialist Myzus persicae (Hemiptera: Aphididae) reveal differential prevalence of maternal effects after host transfer. Bull Entomol Res 97:61–67

    Article  CAS  PubMed  Google Scholar 

  • Puinean AM, Foster SP, Oliphant L, Denholm I, Field LM, Millar NS, Williamson MS, Bass C (2010) Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genet 6:e1000999

    Article  PubMed Central  PubMed  Google Scholar 

  • R Development Core Team (2005) R: a language and environment for statistical computing. Statistical Computing, Vienna, Austria, www.R-project.org

  • Ramsey JS, Jander G (2008) Testing nicotine tolerance in aphids using an artificial diet experiment. J Vis Exp 15:701

    PubMed  Google Scholar 

  • Ramsey JS, Wilson AC, De Vos M, Sun Q, Tamborindeguy C, Winfield A, Malloch G, Smith DM, Fenton B, Gray SM et al (2007) Genomic resources for Myzus persicae: EST sequencing, SNP identification, and microarray design. BMC Genomics 8:423

    Article  PubMed Central  PubMed  Google Scholar 

  • Ramsey JS, Rider DS, Walsh TK, De Vos M, Gordon KHJ, Ponnala L, Macmil SL, Roe BA, Jander G (2010) Comparative analysis of detoxification enzymes in Acrythosiphon pisum and Myzus persicae. Insect Mol Biol 19(Suppl 2):155–164

    Article  CAS  PubMed  Google Scholar 

  • Rao SAK, Carolan JC, Wilkinson TL (2013) Proteomic profiling of cereal aphid saliva reveals both ubiquitous and adaptive secreted proteins. PLoS One 8:e0057413

    Article  Google Scholar 

  • Scott JG, Liu N, Wen Z (1998) Insect cytochromes P450: diversity, insecticide resistance and tolerance to plant toxins. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 121:147–155

    Article  CAS  PubMed  Google Scholar 

  • Shigehara T, Takada H (2003) Changes in genotypic composition of Myzus persicae (Hemiptera: Aphididae) on tobacco during the past two decades in Japan. Bull Entomol Res 93:537–544

    Article  CAS  PubMed  Google Scholar 

  • Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W (eds) Computational biology bolutions using R and Bioconductor. Springer, New York, pp 397–420

    Chapter  Google Scholar 

  • Smyth GK, Speed T (2003) Normalization of cDNA microarray data. Methods 31:265–273

    Article  CAS  PubMed  Google Scholar 

  • Snyder MJ, Feyereisen R (1993) Induction of cytochrome P-450 activities by nicotine in the tobacco hornworm, Manduca sexta. J Chem Ecol 19:2903–2916

    Article  CAS  PubMed  Google Scholar 

  • Thurston R, Smith WT, Cooper BP (1966) Alkaloid secretion by trichomes of Nicotiana species and resistance to aphids. Ent Exp Appl 9:428–432

    Article  CAS  Google Scholar 

  • Will T, Steckbauer K, Hardt M, van Bel AJE (2012) Aphid gel saliva: sheath structure, protein composition and secretory dependence on stylet-tip milieu. PLoS One 7:e0046903

    Article  Google Scholar 

  • Yang Z, Zhang F, He Q, He G (2005) Molecular dynamics of detoxification and toxin-tolerance genes in brown planthopper (Nilaparvata lugens Stal., Homoptera: Delphacidae) feeding on resistant rice plants. Arch Insect Biochem Physiol 59:59–66

    Article  CAS  PubMed  Google Scholar 

  • Zepeda-Paulo FA, Simon JC, Ramirez CC, Fuentes-Contreras E, Margaritopoulos JT, Wilson AC, Sorenson CE, Briones LM, Azevedo R, Ohashi DV et al (2010) The invasion route for an insect pest species: the tobacco aphid in the New World. Mol Ecol 19:4738–4752

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was funded by Binational Science Foundation grant 2007045 to MG and GJ, USDA grant 2012-67013-19350 to GJ, by National Institutes of Health/National Institute of General Medical Sciences grant 5T32GM008500 for research conducted by DAE, and by Carolyn Sampson in the form of a stipend for YX. The authors thank the Cornell Microarray Core Facility for technical assistance.

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Authors and Affiliations

  1. Boyce Thompson Institute, Ithaca, NY, 14853, USA

    John S. Ramsey, Dezi A. Elzinga, Pooja Sarkar, Yi-Ran Xin & Georg Jander

  2. Department of Entomology, Volcani Center, Bet Dagan, 50250, Israel

    Murad Ghanim

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  1. John S. Ramsey
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  2. Dezi A. Elzinga
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  3. Pooja Sarkar
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  4. Yi-Ran Xin
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  5. Murad Ghanim
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  6. Georg Jander
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Corresponding author

Correspondence to Georg Jander.

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Ramsey, J.S., Elzinga, D.A., Sarkar, P. et al. Adaptation to Nicotine Feeding in Myzus persicae . J Chem Ecol 40, 869–877 (2014). https://doi.org/10.1007/s10886-014-0482-5

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  • DOI: https://doi.org/10.1007/s10886-014-0482-5

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