title: Neonicotinoid insecticides alter induced defenses and increase susceptibility to spider mites in distantly related crop plants.
abstract: BACKGROUND
  Chemical suppression of arthropod herbivores is the most common approach to plant protection. Insecticides, however, can cause unintended, adverse consequences for non-target organisms. Previous studies focused on the effects of pesticides on target and non-target pests, predatory arthropods, and concomitant ecological disruptions. Little research, however, has focused on the direct effects of insecticides on plants. Here we demonstrate that applications of neonicotinoid insecticides, one of the most important insecticide classes worldwide, suppress expression of important plant defense genes, alter levels of phytohormones involved in plant defense, and decrease plant resistance to unsusceptible herbivores, spider mites Tetranychus urticae (Acari: Tetranychidae), in multiple, distantly related crop plants.
  
  
  RESULTS
  Using cotton (Gossypium hirsutum), corn (Zea mays) and tomato (Solanum lycopersicum) plants, we show that transcription of phenylalanine ammonia lyase, coenzyme A ligase, trypsin protease inhibitor and chitinase are suppressed and concentrations of the phytohormone OPDA and salicylic acid were altered by neonicotinoid insecticides. Consequently, the population growth of spider mites increased from 30% to over 100% on neonicotinoid-treated plants in the greenhouse and by nearly 200% in the field experiment.
  
  
  CONCLUSIONS
  Our findings are important because applications of neonicotinoid insecticides have been associated with outbreaks of spider mites in several unrelated plant species. More importantly, this is the first study to document insecticide-mediated disruption of plant defenses and link it to increased population growth of a non-target herbivore. This study adds to growing evidence that bioactive agrochemicals can have unanticipated ecological effects and suggests that the direct effects of insecticides on plant defenses should be considered when the ecological costs of insecticides are evaluated.
authors: Department of Entomology, Texas A&M University, College Station, Texas, United States of America. adrianna.szczepaniec@sdstate.edu
authors: Adrianna
authors: A
authors: Szczepaniec
authors: Michael J
authors: MJ
authors: Raupp
authors: Roy D
authors: RD
authors: Parker
authors: David
authors: D
authors: Kerns
authors: Micky D
authors: MD
authors: Eubanks
mesh_terms: D000818:Animals; D002688:Chitinases / Q000037:antagonists & inhibitors / Q000235:genetics / Q000276:immunology; D003066:Coenzyme A Ligases / Q000037:antagonists & inhibitors / Q000235:genetics / Q000276:immunology; D018506:Gene Expression Regulation, Plant / Q000187:drug effects* / Q000276:immunology; D003368:Gossypium / Q000187:drug effects* / Q000276:immunology / Q000469:parasitology; D007306:Insecticides / Q000633:toxicity*; D018551:Solanum lycopersicum / Q000187:drug effects* / Q000276:immunology / Q000469:parasitology; D010650:Phenylalanine Ammonia-Lyase / Q000037:antagonists & inhibitors / Q000235:genetics / Q000276:immunology; D010940:Plant Proteins / Q000037:antagonists & inhibitors / Q000235:genetics / Q000276:immunology*; D011156:Population Density; D040102:Tetranychidae / Q000187:drug effects / Q000502:physiology*; D014158:Transcription, Genetic / Q000187:drug effects; D014361:Trypsin Inhibitors / Q000235:genetics / Q000276:immunology; D003313:Zea mays / Q000187:drug effects* / Q000276:immunology / Q000469:parasitology
chemical_list: D007306:Insecticides; D010940:Plant Proteins; D014361:Trypsin Inhibitors; D002688:Chitinases; D010650:Phenylalanine Ammonia-Lyase; D003066:Coenzyme A Ligases
references: Oecologia. 1997 Dec;113(1):74-81
references: 28307296
references: Pest Manag Sci. 2008 Nov;64(11):1099-105
references: 18561166
references: Annu Rev Entomol. 2003;48:339-64
references: 12208819
references: Mol Ecol. 2004 Jun;13(6):1643-53
references: 15140107
references: Annu Rev Phytopathol. 2005;43:545-80
references: 16078895
references: BMC Bioinformatics. 2006 Feb 22;7:85
references: 16504059
references: Plant Physiol. 2002 Sep;130(1):494-503
references: 12226528
references: Plant Physiol. 2008 Mar;146(3):839-44
references: 18316638
references: Insect Biochem Mol Biol. 2012 Jul;42(7):455-65
references: 22465149
references: Annu Rev Genet. 2010;44:1-24
references: 20649414
references: J Econ Entomol. 2007 Jun;100(3):830-7
references: 17598545
references: Curr Opin Plant Biol. 2003 Aug;6(4):365-71
references: 12873532
references: PLoS One. 2011;6(5):e20018
references: 21655275
references: Ecol Lett. 2006 Oct;9(10):1157-71
references: 16972879
references: Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12837-42
references: 11592974
references: Plant Physiol. 2004 May;135(1):483-95
references: 15122016
references: Proc Natl Acad Sci U S A. 2010 Oct 12;107(41):17527-32
references: 20876120
references: BMC Neurosci. 2011 May 31;12:51
references: 21627790
references: Oecologia. 2009 Mar;159(2):363-76
references: 19002502
references: J Chem Ecol. 2002 Jun;28(6):1131-59
references: 12184393
references: Pest Manag Sci. 2008 Nov;64(11):1084-98
references: 18712805
references: Methods. 2001 Dec;25(4):402-8
references: 11846609
references: Plant Physiol. 2004 Jan;134(1):420-31
references: 14701914
references: Annu Rev Plant Biol. 2008;59:41-66
references: 18031220
references: Annu Rev Entomol. 2010;55:19-38
references: 19961321
references: Pest Manag Sci. 2009 May;65(5):497-503
references: 19206090
references: Exp Appl Acarol. 2013 Mar;59(3):307-18
references: 23007227
references: Plant J. 2009 Jan;57(2):230-42
references: 18801014
references: Plant Physiol. 2004 Aug;135(4):2025-37
references: 15310835