Induced Release of a Plant-Defense Volatile ‘Deceptively’ Attracts Insect Vectors to Plants Infected with a Bacterial Pathogen

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Transmission of plant pathogens by insect vectors is a complex biological process involving interactions between the plant, insect, and pathogen. Pathogen-induced plant responses can include changes in volatile and nonvolatile secondary metabolites as well as major plant nutrients. Experiments were conducted to understand how a plant pathogenic bacterium, Candidatus Liberibacter asiaticus (Las), affects host preference behavior of its psyllid (Diaphorina citri Kuwayama) vector. D. citri were attracted to volatiles from pathogen-infected plants more than to those from non-infected counterparts. Las-infected plants were more attractive to D. citri adults than non-infected plants initially; however after feeding, psyllids subsequently dispersed to non-infected rather than infected plants as their preferred settling point. Experiments with Las-infected and non-infected plants under complete darkness yielded similar results to those recorded under light. The behavior of psyllids in response to infected versus non-infected plants was not influenced by whether or not they were carriers of the pathogen. Quantification of volatile release from non-infected and infected plants supported the hypothesis that odorants mediate psyllid preference. Significantly more methyl salicylate, yet less methyl anthranilate and D-limonene, was released by infected than non-infected plants. Methyl salicylate was attractive to psyllids, while methyl anthranilate did not affect their behavior. Feeding on citrus by D. citri adults also induced release of methyl salicylate, suggesting that it may be a cue revealing location of conspecifics on host plants. Infected plants were characterized by lower levels of nitrogen, phosphorus, sulfur, zinc, and iron, as well as, higher levels of potassium and boron than non-infected plants. Collectively, our results suggest that host selection behavior of D. citri may be modified by bacterial infection of plants, which alters release of specific headspace volatiles and plant nutritional contents. Furthermore, we show in a laboratory setting that this apparent pathogen-mediated manipulation of vector behavior may facilitate pathogen spread.

Vyšlo v časopise: Induced Release of a Plant-Defense Volatile ‘Deceptively’ Attracts Insect Vectors to Plants Infected with a Bacterial Pathogen. PLoS Pathog 8(3): e32767. doi:10.1371/journal.ppat.1002610
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002610

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1. PurcellA 1982 Insect vector relationships with procaryotic plant-pathogens. Ann Rev of Phytopathol 20 397 417

2. PurcellAH 1985 The ecology of bacterial and mycoplasma plant diseases spread by leafhoppers and planthoppers. NaultLRRodriguezJG The leafhoppers and planthoppers New York J Wiley & Sons 351 380

3. EigenbrodeSDingHShielPBergerP 2002 Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc R Soc Lond B Biol Sci 269 455 460

4. Jimenez-MartinezEBosque-PerezNBergerPZemetraRDingH 2004 Volatile cues influence the response of Rhopalosiphum padi (Homoptera: Aphididae) to barley yellow dwarf virus-infected transgenic and untransformed wheat. Environ Entomol 33 1207 1216

5. BelliureBJanssenAMarisPPetersDSabelisM 2005 Herbivore arthropods benefit from vectoring plant viruses. Ecol Lett 8 70 79

6. FereresAMorenoA 2009 Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Res 141 158 168

7. MannRSidhuJButterNSohiASekhonP 2008 Performance of Bemisia tabaci (Hemiptera : Aleyrodidae) on healthy and cotton leaf curl virus infected cotton. Fla Entomol 91 249 255

8. MannRSSidhuJSButterNS 2009 Settling preference of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) on healthy versus cotton leaf curl virus-infected cotton plants. Int J Trop Insect Sci 29 57 61

9. MauckKDe MoraesCMescherM 2010 Deceptive chemical signals induced by a plant virus attracts insect vectors to inferior hosts. Proc Natl Acad Sci U S A 107 3600 3605

10. DaughertyMLopesJAlmeidaR 2010 Vector within-host feeding preference mediates transmission of a heterogeneously distributed pathogen. Ecol Entomol 35 360 366

11. SchoonhovenL 2005 Insect-plant relationships: the whole is more than the sum of its parts. Entomol Exp Appl 115 5 6

12. Jiménez-MartínezESBosque-PérezNABergerPAZemetraRS 2004 Life history of the bird cherryoat aphid, Rhopalosiphum padi (Homoptera: Aphididae), on transgenic and untransformed wheat challenged with Barley yellow dwarf virus. J Econ Entomol 97 203 212

13. CastleSJMowryTMBergerPH 1998 Differential settling by Myzus persicae (Homoptera: Aphididae) on various viruses infected host plants. Ann Entomol Soc Am 91 661 667

14. De BoerJPosthumusMDickeM 2004 Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. J Chem Ecol 34 1045 1049

15. MayerCJVilcinskasAGrossJ 2008a Phytopathogen lures its insect vector by altering host plant odor. J Chem Ecol 34 1518 1522

16. MayerCJVilcinskasAGrossJ 2008b Pathogen-induced release of plant allomone manipulates vector insect behavior. J Chem Ecol 34 1518 1522

17. KoellaJCSrensenFLAndersonRA 1998 The malaria parasite, Plasmodium falciparum, increases the frequency of multiple feeding of its mosquito vector, Anopheles gambiae. Proc R Soc Lond B Biol Sci 265 763 768

18. JiuMZhouXPLiuSS 2006 Acquisition and transmission of two begomoviruses by the B and a non-B biotype of Bemisia tabaci from Zhejiang, China. J Phytopathol 154 587 591

19. Pelz-StelinskiKSBrlanskyRHEbertTARogersME 2010 Transmission parameters for Candidatus Liberibacter asiaticus by Asian citrus psyllid (Hemiptera: Psyllidae). J Econ Entomol 103 1531 1541

20. RoossinckMJ 2011 The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 9 99 108

21. HuangJCardozaYJSchmelzEARainaREngelberthJ 2003 Differential volatile emissions and salicylic acid levels from tobacco plants in response to different strains of Pseudomonas syringae. Planta 217 767 775

22. BoveJM 2006 Huanglongbing: A destructive, newly-emerging, century-old disease of citrus. J Plant Pathol 88 7 37

23. GarnierMDanelNBoveJM 1984 Etiology of citrus greening disease. Ann Inst Pasteur Mic A135 169 179

24. JagoueixSBoveJMGarnierM 1997 Comparison of the 16S/23S ribosomal intergenic regions of “Candidatus Liberobacter asiaticum” and “Candidatus Liberobacter africanum,” the two species associated with citrus huanglongbing (greening) disease. Int J Syst Bacteriol 47 224 227

25. HocquelletAToorawaPBoveJMGarnierM 1999 Detection and identification of the two Candidatus Liberobacter species associated with citrus huanglongbing by PCR amplification of ribosomal protein genes of the beta operon. Mol Cell Probe 13 373 379

26. SagaramUSDeAngelisKMTrivediPAndersenGLLuS-E 2009 Bacterial diversity analysis of huanglongbing pathogen-infected citrus, using phylochip arrays and 16S rRNA gene clone library sequencing. Appl Environ Microbiol 75 1566 1574

27. ChristensenNMNicolaisenMHansenMSchulzA 2004 Distribution of phytoplasmas in infected plants as revealed by real-time PCR and bioimaging. Mol Plant Microbe Int 17 1175 1184

28. HalbertSEManjunathKL 2004 Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: A literature review and assessment of risk in Florida. Fla Entomol 87 330 353

29. LopesSABertoliniEFrareGFMartinsECWulffNA 2009 Graft transmission efficiencies and multiplication of ‘Candidatus Liberibacter americanus’ and ‘Ca. Liberibacter asiaticus’ in citrus Plants. Phytopathology 99 301 306

30. CapoorSPRaoDGViswanathSM 1974 Greening disease of citrus in the Deccan Trap Country and its relationship with the vector, Diaphorina citri Kuwayama. Proc Sixth Conf IOCV 43 49

31. RoistacherCN 1991 Greening. RoistacherCN Techniques for biological detection of specific citrus graft transmissible diseases Rome Food and Agricultural Organization of the United Nations 35 45

32. HungTHHungSCChenCNHsuMHSuHJ 2004 Detection by PCR of Candidatus Liberibacter asiaticus, the bacterium causing citrus huanglongbing in vector psyllids: application to the study of vector-pathogen relationships. Plant Pathol 53 96 102

33. InoueHOhnishiJItoTTomimuraKMiyataS 2009 Enhanced proliferation and efficient transmission of Candidatus Liberibacter asiaticus by adult Diaphorina citri after acquisition feeding in the nymphal stage. Ann Appl Biol 155 29 36

34. MollJNMartinMM 1973 Electron microscope evidence that citrus psylla Trioza-erytreae is a vector of greening disease in South Africa. Phytophylactica 5 41 44

35. McCleanAPDSchwarzRE 1970 Greening or blotchy-mottle disease of citrus. Phytophylactica 2 177 193

36. TiwariSLewis-RosenblumHPelz-StelinskiKStelinskiLL 2010 Incidence of Candidatus Liberibacter asiaticus infection in abandoned citrus occurring in proximity to commercially managed groves. J Econ Entomol 103 1972 1978

37. WenningerEJHallDG 2007 Daily timing of mating and age at reproductive maturity in Diaphorina citri (Hemiptera: Psyllidae). Fla Entomol 90 715 722

38. WenningerEJHallDG 2008 Importance of multiple mating to female reproductive output in Diaphorina citri. Physiol Entomol 33 316 321

39. WenningerEJStelinskiLLHallDG 2009 Roles of olfactory cues, visual cues, and mating status in orientation of Diaphorina citri Kuwayama (Hemiptera: Psyllidae) to four different host plants. Environ Entomol 38 225 234

40. PattJMSetamouM 2010 Responses of the Asian citrus psyllid to volatiles emitted by the flushing shoots of its rutaceous host plants. Environ Entomol 39 618 624

41. ParePWTumlinsonJH 1999 Plant volatiles as a defense against insect herbivores. Plant Physiol 121 325 331

42. HolopainenJK 2004 Multiple functions of inducible plant volatiles. Trends Plant Sci 9 529 533

43. MummRPosthumusMADickeM 2008 Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. Plant Cell Environ 31 575 585

44. WallingLL 2000 The myriad plant responses to herbivores. J Plant Growth Regul 19 195 216

45. KesslerABaldwinIT 2001 Defensive function of herbivore-induced plant volatile emissions in nature. Science 291 2141 2144

46. KostCHeilM 2006 Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J Ecol 94 619 628

47. StoutMJThalerJSThommaB 2006 Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Ann Rev Entomol 51 663 689

48. WeiJWangLZhuJZhangSNandiOI 2007 Plants attract parasitic wasps to defend themselves against insect pests by releasing hexenol. Plos One 2 e852

49. LiuGJiYBhuiyanNHPilotGSelvarajG 2010 Amino acid homeostasis modulates salicylic acid-associated redox status and defense responses in Arabidopsis. Plant Cell 22 3845 3863

50. GriebelTZeierJ 2010 A role for beta-sitosterol to stigmasterol conversion in plant-pathogen interactions. Plant J 63 254 268

51. MishinaTEZeierJ 2007 Bacterial non-host resistance: interactions of Arabidopsis with non-adapted Pseudomonas syringae strains. Physiola Plantarum 131 448 461

52. MishinaTEZeierJ 2007 Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J 50 500 513

53. MishinaTEGriebelTGeueckeMAttaranEZeierJ 2008 New insights into the molecular events underlying systemic acquired resistance. In: Volume 6 Proceedings of the 13th International Congress on Molecular Plant-Microbe Interactions, Biology of plant-microbe interactions; 21–27 July 2007; Sorrento, Italy 81

54. DeanJVDelaneySP 2008 Metabolism of salicylic acid in wild-type, ugt74f1 and ugt74f2 glucosyltransferase mutants of Arabidopsis thaliana. Physiol Plantarum 132 417 425

55. AttaranEZeierTEGriebelTZeierJ 2009 Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21 954 971

56. ThalerJSAgrawalAAHalitschkeR 2010 Salicylate-mediated interactions between pathogens and herbivores. Ecology 91 1075 1082

57. SistersonMS 2008 Effects of insect-vector preference for healthy or infected plants on pathogen spread: Insights from a model. J Econ Entomol 101 1 8

58. SrininvasanRAlvarezJMEigenbrodeSDBosque-PerezNA 2006 Influence of hairy nightshade Solanum sarrachoides (Sendtner) and Potato leafroll virus (Luteoviridae : Polerovirus) on the host preference of Myzus persicae (Sulzer) (Homoptera : Aphididae). Environ Entomol 35 546 553

59. NgumbiEEigenbrodeSDBosque-PerezNADingHRodriguezA 2007 Myzus persicae is arrested more by blends than by individual compounds elevated in headspace of PLRV-Infected potato. J Chem Ecol 33 1733 1747

60. RoderGRahierMNaisbitRE 2011 Do induced responses mediate the ecological interactions between the specialist herbivores and phytopathogens of an alpine plant? Plos One 6 e19571

61. AjayiODewarAM 1983 The effects of barley yellow dwarf virus, aphids and honeydew on cladosporium infection of winter-wheat and barley. Ann Appl Biol 102 57 65

62. FereresAKampmeierGEIrwinME 1999 Aphid attraction and preference for soybean and pepper plants infected with potyviridae. Ann Entomol Soc Am 92 542 548

63. MarucciRCLopesJRSVendramimJDCorrenteJE 2005 Influence of Xylella fastidiosa infection of citrus on host selection by leafhopper vectors. Entomol Exp Appl 117 95 103

64. StraussE 2009 Phytoplasma research begins to bloom. Science 325 388 390

65. DugoGDi GiacomoA 2002 Citrus: The genus citrus. medicinal and aromatic plants-industrial profiles series New York Taylor & Francis Group, CRC Press 504

66. JabalpurwalaFASmootJMRouseffRL 2009 A comparison of citrus blossom volatiles. Phytochem 70 1428 1434

67. LinSYRoanSFLeeCLChenIZ 2010 Volatile organic components of fresh leaves as indicators of indigenous and cultivated citrus species in Taiwan. Biosci, Biotechnol, Biochem 74 806 811

68. WebsterBBruceTJAPickettJAHardieJ 2008 Olfactory recognition of host plants in the absence of host-specific volatile compounds. Commun Integr Biol 1 167 169

69. WebsterBBruceTJAPickettJAHardieJ 2010 Volatiles functioning as host cues in a blend become nonhost cues when presented alone to the black bean aphid. Anim Behav 79 451 457

70. MaciasWMinkGI 1969 Preference of green peach aphids for virus-infected sugarbeet leaves. J Econ Entomol 62 28 99

71. BluaMJPerringTM 1992 Effects of zucchini yellow mosaic-virus on colonization and feeding-behavior of Aphis-gossypii (Homoptera, Aphididae) alatae. Environ Entomol 21 578 585

72. KaloshianIWallingLL 2005 Hemipterans as plant pathogens. Ann Rev Phytopathol 43 491 521

73. MusserROCipolliniDFHum-MusserSMWilliamsSABrownJK 2005 Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in Solanaceous plants. Arch Insect Biochem Physiol 58 128 137

74. RyalsJANeuenschwanderUHWillitsMGMolinaASteinerHY 1996 Systemic Acquired Resistance. Plant Cell 8 1809 1819

75. DurrantWEDongX 2004 Systemic acquired resistance. Ann Rev Phytopathol 42 185 209

76. ZarateSIKempemaLAWallingLL 2007 Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143 866 875

77. WallingLL 2008 Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146 859 866

78. MontllorCBGildowFE 1986 Feeding responses of two grain aphids to barley yellow dwarf virus-infected oats. Entomol Exp Appl 42 63 69

79. CastleSJBergerPH 1993 Rates of growth and increase of Myzus persicae om virus-infected potatoes according to type of virus-vector relationship. Entomol Exp Appl 69 51 60

80. McElhanyPRealLAPowerAG 1995 Vector preference and disease dynamics: a study of barley yellow dwarf virus. Ecology 76 444 457

81. HubertyAFDennoRF 2006 Consequences of nitrogen and phosphorus limitation for the performance of two planthoppers with divergent life-history strategies. Oecologia 149 444 455

82. HonekA 1991 Environment stress, plant-quality and abundance of cereal aphids (hom, aphididae) on winter-wheat. J Appl Entomol 112 65 70

83. HonekA 1991 Nitrogen-fertilization and abundance of the cereal aphids Metopolophium dirhodum and Sitobion avenae (Homoptera, Aphididae). Z Pflanzenk Pflanzen 98 655 660

84. VanemdenHF 1966 Studies on relations of insect and host plant .3. a comparison of reproduction of Brevicoryne brassicae and Myzus persicae (hemiptera - aphididae) on brussels sprout plants supplied with different rates of nitrogen and potassium. Entomol Exp Appl 9 444 460

85. KerslakeJEWoodinSJHartleySE 1998 Effects of carbon dioxide and nitrogen enrichment on a plant-insect interaction: the quality of Calluna vulgaris as a host for Operophtera brumata. New Phytol 140 43 53

86. AyresMPWilkensRTRuelJJLombarderoMJValleryE 2000 Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi. Ecology 81 2198 2210

87. BentzJATownsendAM 2001 Leaf element content and utilization of maple and elm as hosts by the potato leafhopper (Homoptera: Cicadellidae). Environ Entomol 30 533 539

88. SternerRElserJ 2002 Ecological stoichiometry: The biology of elements from molecules to the biosphere New Jersey Princeton University Press 584

89. ChaboussouF 2004 Healthy crops: A new agricultural revolution Charlbury, UK Jon Carpenter Publishing 244

90. MyersSWGrattonCWolkowskiRPHoggDBWedbergJL 2005 Effect of soil potassium availability on soybean aphid (Hemiptera: Aphididae) population dynamics and soybean yield. J Econ Entomol 98 113 120

91. WalterAJDiFonzoCD 2007 Soil potassium deficiency affects soybean phloem nitrogen and soybean aphid populations. Environ Entomol 36 26 33

92. NomaTGrattonCColunca-GarciaMBrewerMJMuellerEE 2010 Relationship of soybean aphid (Hemiptera: Aphididae) to soybean plant nutrients, landscape structure, and natural enemies. Environ Entomol 39 31 41

93. WeibullJMelinG 1990 Free amino acid content of phloem sap from Brassica plants in relation to performance of Lipaphis erysimi (Hemiptera: Aphididae). Ann Appl Biol 116 417 423

94. BluaMJPerringTMMadoreMA 1994 Plant virus-induced changes in aphid population development and temporal fluctuations in plant nutrients. J Chem Ecol 20 691 707

95. FanJChenCBrlanskyRHGmitterFGJrLiZG 2010 Changes in carbohydrate metabolism in Citrus sinensis infected with ‘Candidatus Liberibacter asiaticus’. Plant Pathol 59 1037 1043

96. HaoPLiuCWangYChenRTangM 2008 Herbivore-induced callose deposition on the sieve plates of rice: An important mechanism for host resistance. Plant Physiol 146 1810 1820

97. HartungJSHalbertSEPelz-StelinskiKSBrlanskyRHChenC 2010 Lack of evidence for transmission of ‘Candidatus liberibacter asiaticus’ through citrus seed taken from affected fruit. Plant Dis 94 1200 1205

98. LiWBHartungJSLevyL 2006 Quantitative real-time PCR for detection and identification of Candidatus Liberibacter species associated with citrus huanglongbing. J Microbiol Meth 66 104 115

99. ThaoMLBaumannP 2000 Evolutionary relationships of psyllid endosymbionts based on 16S rDNA, 23S rDNA and atpAGD analyses. Abstracts of the General Meeting of the American Society for Microbiology 100 632

100. MannRSRouseffRLSmootJMCastleWSStelinskiLL 2011 Sulfur volatiles from Allium spp. affect Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), response to citrus volatiles. Bull Entomol Res 101 89 97

101. BriscoeADChittkaL 2001 The evolution of color vision in insects. Ann Rev Entomol 46 471 510

102. NauenRElbertA 1997 Apparent tolerance of a field-collected strain of Myzus nicotianae to imidacloprid due to strong antifeeding responses. Pestic Sci 49 252 258

103. BoinaDROnagbolaEOSalyaniMStelinskiLL 2009 Antifeedant and sublethal effects of imidacloprid on Asian citrus psyllid, Diaphorina citri. Pest Manag Sci 65 870 877

104. AuclairJL 1959 The influence of dietary amino acids on the blood amino acids of the German cockroach, Blattella germanica (L.). J Insect Physiol 3 127 31

105. PaguiaPPathakMDHeinrichsEA 1980 Honeydew excretion measurement techniques for determining differential feeding activity of biotypes of Nilaparvata lugens on rice varieties. J Econ Entomol 73 35 40

106. NisbetAJWoodfordJATStrangRHC 1994 Quantifying aphid feeding on non-radioactive food sources. Entomol Exp Appl 72 85 89