Evaluating Insect-Microbiomes at the Plant-Insect Interface

Journal of Chemical Ecology

Volumn 40, Issue 7, 2014, Pages 836-847

  Casteel, Clare L ^a   Hansen, Allison K ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Defense; Effectors; PAMPs; Phytohormones; Plant insect interactions; Symbiont

Indexed keywords

BIOINFORMATICS; HORMONE; HOST PLANT; INTERSPECIFIC INTERACTION; MICROBIAL COMMUNITY; PHYTOCHEMISTRY; PLANT DEFENSE; PLANT-INSECT INTERACTION; SYMBIOSIS; SYNERGISM;

HEXAPODA;

PHYTOHORMONE; VEGETABLE PROTEIN;

ANIMAL; HERBIVORY; HOST PATHOGEN INTERACTION; INSECT; METABOLISM; MICROBIOLOGY; MICROFLORA; PARASITOLOGY; PHYSIOLOGY; PLANT; SIGNAL TRANSDUCTION;

ANIMALS; HERBIVORY; HOST-PATHOGEN INTERACTIONS; INSECTS; MICROBIOTA; PLANT GROWTH REGULATORS; PLANT PROTEINS; PLANTS; SIGNAL TRANSDUCTION;

EID: 84906081446     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-014-0475-4     Document Type: Review

References (105)

1. Armijos Jaramillo VD, Vargas WA, Sukno SA, Thon MR (2013) New insights into the evolution and structure of Colletotrichum Plant-Like Subtilisins (CPLSs). Comm & Integ Biol 6: e25727. doi: 10. 4161/cib. 25727.
2. Baldwin IT (2010) Plant volatiles. Curr Biol 20: 392-397. doi: 10. 1016/j. cub. 2010. 02. 052.
3. Bardoel BW, Strijp JA (2011) Molecular battle between host and bacterium: recognition in innate immunity. J Mol Recogn 24: 1077-1086. doi: 10. 1002/jmr. 1156.
4. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69: 473-488. doi: 10. 1007/s11103-008-9435-0.
5. Barr KL, Hearne LB, Briesacher S, Clark TL, Davis GE (2010) Microbial symbionts in insects influence down-regulation of defense genes in maize. PLoS One 5: e11339. doi: 10. 1371/journal. pone. 0011339.
6. Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59: 443-465. doi: 10. 1146/annurev. arplant. 58. 032806. 103805.
7. Body M, Kaiser W, Dubreuil G, Casas J, Giron D (2013) Leaf-miners co-opt microorganisms to enhance their nutritional environment. J Chem Ecol 39: 969-977. doi: 10. 1007/s10886-013-0307-y.
8. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406. doi: 10. 1146/annurev. arplant. 57. 032905. 105346.
9. Brault V, Uzest M, Monsion B, Jacquot E, Blanc S (2010) Aphids as transport devices for plant viruses. C R Biol 333(6-7): 524-538. doi: 10. 1016/j. crvi. 2010. 04. 001.
10. Casteel CL, Jander G (2013) New synthesis: investigating mutualisms in virus-vector interactions. J Chem Ecol 39: 809.
11. Casteel CL, Hansen AK, Walling LL, Paine TD (2012) Manipulation of plant defense responses by the tomato psyllid (Bactericerca cockerelli) and its associated endosymbiont Candidatus Liberibacter psyllaurous. PLoS One 7: e35191. doi: 10. 1371/journal. pone. 0035191.
12. Casteel CL, Yang C, Nanduri AC, Whitham SA, Jander G (2014) The Nia-Pro protein of turnip mosaic virus improves growth and reproduction of the aphid vector, Myzus persicae (green peach aphid). Plant J 77: 653-663.
13. Castro MM, Tanus-Santos JE (2013) Inhibition of matrix metalloproteinases (MMPs) as a potential strategy to ameliorate hypertension-induced cardiovascular alterations. Curr Drug Targets 14: 335-343.
14. Chaudhary R, Atamian HS, Shen Z, Briggs SP, Kaloshian I (2014) GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense. Proc Natl Acad Sci U S A 111(24): 8919-8924.
15. Chen Z, Agnew JL, Cohen JD, He P, Shan L, Sheen J, Kunkel BN (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc Natl Acad Sci U S A 104: 20131-20136. doi: 10. 1073/pnas. 0704901104.
16. Choi J, Huh SU, Kojima M, Sakakibara H, Paek KH, Hwang I (2010) The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis. Dev Cell 19: 284-295. doi: 10. 1016/j. devcel. 2010. 07. 011.
17. Choi J, Choi D, Lee S, Ryu CM, Hwang I (2011) Cytokinins and plant immunity: old foes or new friends? Trends Plant Sci 16: 388-394. doi: 10. 1016/j. tplants. 2011. 03. 003.
18. Chu C-C, Spencer JL, Curzi MJ, Zavala JA, Seufferheld MJ (2013) Gut bacteria facilitate adaptation to crop rotation in the western corn rootworm. Proc Natl Acad Sci U S A 110: 11917-11922. doi: 10. 1073/pnas1301886110.
19. Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF, Hoover K, Luthe DS, Felton GW (2013) Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci U S A 110: 15728-15733. doi: 10. 1073/pnas. 1308867110.
20. Cleland CF, Ajami A (1974) Identification of the flower-inducing factor isolated from aphid honeydew as being salicylic acid. Plant Physiol 54: 904-906.
21. Colman DR, Toolson EC, Takacs-Vesbach CD (2012) Do diet and taxonomy influence insect gut bacterial communities? Mol Ecol 21: 5124-5137. doi: 10. 1111/j. 1365-294x. 2012. 05752. x.
22. Cui H, Bahrami AK, Pringle EG, Hernadez-Guzman G, Bender CL, Pierce NE, Ausubel F (2005) Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc Natl Acad Sci U S A 102: 1791-1796.
23. Cui H, Xiang T, Zhou JM (2009) Plant immunity: a lesson from pathogenic bacterial effector proteins. Cellu Microbiol 11: 1453-1461. doi: 10. 1111/j. 1462-5822. 2009. 01359. x.
24. Daborn PJ, Waterfield N, Silva CP, Au C, Sharma S, Ffrench-Constant RH (2002) A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proc Natl Acad Sci U S A 99: 10742-10747. doi: 10. 1073/pnas. 10268099.
25. Dale C, Moran NA (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126: 453-465. doi: 10. 1016/j. cell. 2006. 07. 014.
26. Dale C, Young SA, Haydon DT, Welburn SC (2001) The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc Natl Acad Sci U S A 13(98): 1883-1888.
27. Dale C, Plague GR, Wang B, Ochman H, Moran NA (2002) Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc Natl Acad Sci U S A 99: 12397-12402. doi: 10. 1073/pnas. 182213299.
28. Davis TS, Horton DR, Munyaneza JE, Landolt PJ (2012) Experimental infection of plants with an herbivore-associated bacterial endosymbiont influences herbivore host selection behavior. PLoS One 7: e49330. doi: 10. 1371/journal. pone. 0049330.
29. Doares SH, Narvaez-Vasquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108(4): 1741-1746.
30. Durbak A, Yao H, McSteen P (2012) Hormone signaling in plant development. Curr Opin Plant Biol 15(1): 92-96. doi: 10. 1016/j. pbi. 2011. 12. 004.
31. 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.
32. Engel P, Moran NA (2013) The gut microbiota of insects - diversity in structure and function. FEMS Microbiol Rev 37: 699-735. doi: 10. 1111/1574-6976. 12025.
33. Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17: 250-259. doi: 10. 1016/j. tplants. 2012. 01. 003.
34. Filichkin SA, Brumfield S, Filichkin TP, Young MJ (1997) In vitro interactions of the aphid endosymbiotic SymL chaperonin with barley yellow dwarf virus. J Virol 71: 569-577.
35. Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64: 839-863. doi: 10. 1146/annurev-arplant-042811-105606.
36. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopath 43: 205-227.
37. Glickmann E, Garden L, Jacquet S, Hussain S, Elasri M, Petit A, Dessaux Y (1998) Auxin produciton is a common feature of most pathovars of Pseudomonas syringae. Mol Plant Microbe Interact 11: 156-162.
38. Hansen AK, Moran NA (2013) The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol Ecol 23: 1473-1496. doi: 10. 1111/mec. 12421.
39. Hansen AK, Trumble JT, Stouthamer R, Paine TD (2008) A new huanglongbing species, "Candidatus Liberibacter psyllaurous" found to infect tomato and potato, is vectored by the psyllid Bactericera cockerelli (Sulc). App Environ Microbiol 74: 5862-5865. doi: 10. 1128/aem. 01268-08.
40. Hansen AK, Vorburger C, Moran NA (2012) Genomic basis of endosymbiont-conferred protection against an insect parasitoid. Genome Res 22: 106-114. doi: 10. 1101/gr. 125351. 111.
41. Hare JD (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Entomol 56: 161-180. doi: 10. 1146/annurev-ento-120709-144753.
42. Henry E, Yadeta KA, Coaker G (2013) Recognition of bacterial plant pathogens: local, systemic and transgenerational immunity. New Phytol 199: 908-915. doi: 10. 1111/nph. 12214.
43. Hirakata Y, Kaku M, Mizukane R, Ishida K, Furuya N, Matsumoto T, Tateda K, Yamaguchi K (1992) Potential effects of erythromycin on host defense systems and virulence of Pseudomonas aeruginosa. Antimicrob Agents Chemother 36: 1922-1927.
44. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59: 41-66. doi: 10. 1146/annurev. arplant. 59. 032607. 092825.
45. Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J, Tholl D (2012) The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-beta-caryophyllene, is a defense against a bacterial pathogen. New Phytol 193: 997-1008. doi: 10. 1111/j. 1469-8137. 2011. 04001. x.
46. Husnik F, Nikoh N, Koga R, Ross L, Duncan RP, Fujie M, Tanaka M, Satoh N, Bachtrog D, Wilson ACC, von Dohlen CD, Fukatsu T, McCutcheon JP (2013) Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153: 1567-1578.
47. Hussain A, Forrest JM, Dixon AF (1974) Sugar, organic acid, phenolic acid and plant growth regulator content of extracts of honeydew of the aphid Myzus persicae and of its host plant, Raphanus sativus. Ann Appl Biol 78: 65-73.
48. Hwang HH, Wang MH, Lee YL, Tsai YL, Li YH, Yang FJ, Liao YC, Lin SK, Lai EM (2010) Agrobacterium-produced and exogenous cytokinin-modulated Agrobacterium-mediated plant transformation. Mol Plant Pathol 11: 677-690. doi: 10. 1111/j. 1364-3703. 2010. 00637. x.
49. Jameson P (2000) Cytokinins and auxins in plant-pathogen interactions - an overview. Plant Growth Regul 32: 369-380.
50. Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329. doi: 10. 1038/nature05286.
51. Kaiser W, Huguet E, Casas J, Commin C, Giron D (2010) Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proc Biol Sci 277: 2311-2319. doi: 10. 1098/rspb. 2010. 0214.
52. Kollner TG, Held M, Lenk C, Hiltpold I, Turlings TC, Gershenzon J, Degenhardt J (2008) A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20: 482-494. doi: 10. 1105/tpc. 107. 051672.
53. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, van Loon LC, Pieterse CM (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147: 1358-1368. doi: 10. 1104/pp. 108. 121392.
54. Langenheim JH (1994) Higher plant terpenoids: a phytocentric overview of their ecological roles. J Chem Ecol 20: 1223-1280. doi: 10. 1007/bf02059809.
55. Leon-Reyes A, Du Y, Koornneef A, Proietti S, Korbes AP, Memelink J, Pieterse CM, Ritsema T (2010a) Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Mol Plant Microbe Interact 23: 187-197. doi: 10. 1094/mpmi-23-2-0187.
56. Leon-Reyes A, van der Does D, De Lange ES, Delker C, Wasternack C, van Wees SCM, Ritsema T, Pieterse CMJ (2010b) Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta (Berlin) 232: 1423-1432. doi: 10. 1007/s00425-010-1265-z.
57. Leroy PD, Sabri A, Heuskin S, Thonart P, Lognay G, Verheggen FJ, Francis F, Brostaux Y, Felton GW, Haubruge E (2011) Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies. Nat Commun 2: 348. doi: 10. 1038/ncomms1347.
58. Mann RS, Ali JG, Hermann SL, Tiwari S, Pelz-Stelinski KS, Alborn HT, Stelinski LL (2012) Induced release of a plant-defense volatile 'deceptively' attracts insect vectors to plants infected with a bacterial pathogen. PLoS Pathog 8: e1002610. doi: 10. 1371/journal. ppat. 1002610.
59. Mauck KE, De Moraes CM, Mescher MC (2010) Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proc Natl Acad Sci U S A 107: 3600-3605.
60. Mauck K, Bosque-Pérez NA, Eigenbrode SD et al (2012) Transmission mechanisms shape pathogen effects on host-vector interactions: evidence from plant viruses. Funct Ecol 26: 1162-1175.
61. McCutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10: 13-26. doi: 10. 1038/nrmicro2670.
62. McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci 110: 3229-3236. doi: 10. 1073/pnas. 1218525110.
63. McSteen P, Zhao Y (2008) Plant hormones and signaling: common themes and new developments. Dev Cell 14: 467-473. doi: 10. 1016/j. devcel. 2008. 03. 013.
64. Mithofer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63: 431-450. doi: 10. 1146/annurev-arplant-042110-103854.
65. Mukhtar MS, Carvunis A-R, Dreze M, Epple P, Steinbrenner J, Moore J, Tasan M, Galli M, Hao T, Nishimura MT, Pevzner SJ, Donovan SE, Ghamsari L, Santhanam B, Romero V, Poulin MM, Gebreab F, Gutierrez BJ, Tam S, Monachello D, Boxem M, Harbort CJ, McDonald N, Gai L, Chen H, He Y, Consortium EUE, Vandenhaute J, Roth FP, Hill DE, Ecker JR, Vidal M, Beynon J, Braun P, Dangl JL (2011) Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333: 596-601. doi: 10. 1126/science. 1203659.
66. Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140: 249-262.
67. Ng TF, Duffy S, Polston JE et al (2011) Exploring the diversity of plant DNA viruses and their satellites using vector-enabled metagenomics on whiteflies. PLoS One 6: e19050.
68. Nikolaidis N, Doran N, Cosgrove DJ (2014) Plant expansins in bacteria and fungi: evolution by horizontal gene transfer and independent domain fusion. Mol Biol Evol 31: 376-386. doi: 10. 1093/molbev/mst206.
69. Ochman H, Moran NA (2001) Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292: 1096-1099. doi: 10. 1126/science. 1058543.
70. Ochman H, Lerat E, Daubin V (2005) Examining bacterial species under the specter of gene transfer and exchange. Proc Natl Acad Sci USA 1: 6595-65959.
71. Oliver KM, Degnan PH, Hunter MS, Moran NA (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325: 992-994. doi: 10. 1126/science. 1174463.
72. Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55: 247-266. doi: 10. 1146/annurev-ento-112408-085305.
73. Oliver KM, Smith AH, Russell JA (2013) Defensive symbiosis in the real world - advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct Ecol 28: 341-355. doi: 10. 1111/1365-2435. 12133.
74. Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Canad J Microbiol 42: 207-220.
75. Perilli S, Moubayidin L, Sabatini S (2010) The molecular basis of cytokinin function. Curr Opin Plant Biol 13: 21-26. doi: 10. 1016/j. pbi. 2009. 09. 018.
76. Pertry I, Vaclavikova K, Depuydt S, Galuszka P, Spichal L, Temmerman W, Stes E, Schmulling T, Kakimoto T, van Montagu MC, Strnad M, Holsters M, Tarkowski P, Vereecke D (2009) Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant. Proc Natl Acad Sci U S A 106: 929-934. doi: 10. 1073/pnas. 0811683106.
77. Pieterse CM, van der Does D, Zamioudis C, Leon-Reyes A, van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28: 489-521. doi: 10. 1146/annurev-cellbio-092910-154055.
78. Pitino M, Hogenhout SA (2012) Aphid protein effectors promote aphid colonization in a plant species-specific manner. Mol Plant Microbe Interact 26: 130-139. doi: 10. 1094/MPMI-07-12-0172-FI.
79. Pontes MH, Smith KL, De Vooght L, van den Abbeele J, Dale C (2011) Attenuation of the sensing capabilities of PhoQ in transition to obligate insect-bacterial association. PLoS Genet 7: e1002349-e1002349. doi: 10. 1371/journal. pgen. 1002349.
80. Rasmann S, Kollner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TC (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434(7034): 732-737. doi: 10. 1038/nature03451.
81. Robert CA, Frank DL, Leach KA, Turlings TC, Hibbard BE, Erb M (2013) Direct and indirect plant defenses are not suppressed by endosymbionts of a specialist root herbivore. J Chem Ecol 39: 507-515. doi: 10. 1007/s10886-013-0264-5.
82. Robert-Seilaniantz A, Navarro L, Bari R, Jones JD (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10: 372-379. doi: 10. 1016/j. pbi. 2007. 06. 003.
83. Roossinck MJ (2012) Plant virus metagenomics: biodiversity and ecology. Annu Rev Gen 46: 359-369. doi: 10. 1146/annurev-genet-110711-155600.
84. Roossinck MJ, Saha P, Wiley GB et al (2010) Ecogenomics: using massively parallel pyrosequencing to understand virus ecology. Mol Ecol 19(Suppl 1): 81-88.
85. Sabri A, Vandermoten S, Leroy PD, Haubruge E, Hance T, Thonart P, De Pauw E, Francis F (2013) Proteomic investigation of aphid honeydew reveals an unexpected diversity of proteins. PLoS One 8: e74656. doi: 10. 1371/journal. pone. 0074656.
86. Satchell KJFK (2011) Structure and function of MARTX toxins and other large repetitive RTX proteins. Annu Rev Microbiol 65: 71-90. doi: 10. 1146/annurev-micro-090110-102943.
87. Sloan DB, Nakabachi A, Richards S, Murali SC, Gibbs RA, Moran NA (2014) Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Mol. Biol. Evol.: Oxford University Press. pp 857-871.
88. Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect in Biol 3. doi: 10. 1101/cshperspect. a001438.
89. Stafford CA, Walker GP, Ullman DE (2011) Infection with a plant virus modifies vector feeding behavior. Proc Natl Acad Sci 108: 9350-9355.
90. Stes E, Vandeputte OM, El Jaziri M, Holsters M, Vereecke D (2011) A successful bacterial coup d'etat: how Rhodococcus fascians redirects plant development. Annu Rev Phytopathol 49: 69-86. doi: 10. 1146/annurev-phyto-072910-095217.
91. Stobbe AH, Roossinck MJ (2014) Plant virus metagenomics: what we know and why we need to know more. Front Plant Sci 5: 150.
92. Stout MJ, Thaler JS, Thomma BP (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu Rev Entomol 51: 663-689. doi: 10. 1146/annurev. ento. 51. 110104. 151117.
93. Sugio A, Kingdom HN, MacLean AM, Grieve VM, Hogenhout SA (2011) Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proc Natl Acad Sci USA 1081254-1263. doi: 10. 1073/pnas. 1105664108.
94. Vandermoten S, Harmel N, Mazzucchelli G, De Pauw E, Haubruge E, Francis F (2014) Comparative analyses of salivary proteins from three aphid species. Insect Mol Biol 23: 67-77.
95. Veit B (2009) Hormone mediated regulation of the shoot apical meristem. Plant Mol Biol 69: 397-408. doi: 10. 1007/s11103-008-9396-3.
96. Verhage A, van Wees SCM, Pieterse CMJ (2010) Plant immunity: it's the hormones talking, but what do they say? Plant Physiol 154: 536-540. doi: 10. 1104/pp. 110. 161570.
97. Vlot AC, Klessig DF, Park SW (2008) Systemic acquired resistance: the elusive signal (s). Curr Opin Plant Biol 11: 436-442. doi: 10. 1016/j. pbi. 2008. 05. 003.
98. Vorholt JA (2012) Microbial life in the phyllosphere. Nature Publishing Gr 10: 828-840. doi: 10. 1038/nrmicro2910.
99. Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146: 859-866. doi: 10. 1104/pp. 107. 113142.
100. Walling LL (2009) Adaptive defense responses to pathogens and insects. In: VanLoon LC (ed) Plant innate immunity, vol 51. Advances in Botanical Research, p 551-612. doi: 10. 1016/s0065-2296(09)51013-0.
101. Weech MH, Chapleau M, Pan L, Ide C, Bede JC (2008) Caterpillar saliva interferes with induced Arabidopsis thaliana defence responses via the systemic acquired resistance pathway. J Exp Bot 59: 2437-2448. doi: 10. 1093/jxb/ern108.
102. Werner T, Schmulling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12: 527-538. doi: 10. 1016/j. pbi. 2009. 07. 002.
103. Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143: 866-875.
104. Zhang P, Zhu X, Huang F, Liu Y, Zhang J, Lu Y, Ruan Y (2011) Suppression of jasmonic acid-dependent defense in cotton plant by the Mealybug Phenacoccus solenopsis. PLoS One 6: e22378. doi: 10. 1371/journal. pone. 0022378.
105. Zhang PJ, Li WD, Huang F, Zhang JM, Xu FC, Lu YB (2013) Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting salicylic acid signaling. J Chem Ecol 39: 612-619. doi: 10. 1007/s10886-013-0283-2.