Advertisement

Arthropod-Plant Interactions

, Volume 12, Issue 3, pp 401–413 | Cite as

Interactive effects of aphid feeding and virus infection on host gene expression and volatile compounds in salt-stressed soybean, Glycine max (L.) Merr.

  • Alma G. Laney
  • Pengyin Chen
  • Kenneth L. Korth
Original Paper
  • 163 Downloads

Abstract

Saline soils are becoming an important limiting factor in production agriculture. Soybean cultivars [Glycine max (L.) Merr.] differ in their ability to tolerate salt stress with those that cannot limit ion uptake into leaves being salt sensitive. Those that can partially limit ion uptake into leaves are generally more salt tolerant. Soybean mosaic virus (SMV) is an important viral pathogen of soybean worldwide and is commonly transmitted by the soybean aphid, Aphis glycines Matsumura. In this study, we investigate the interaction of salt stress in soybean with SMV infection and infestation by the soybean aphid by measuring aphid populations in a no-choice assay, gene expression levels, and the induction of volatile organic compounds using static headspace GC–MS analysis. Salt stress and SMV infection both reduced total aphid populations, though SMV did not reduce the total number of aphids per gram of fresh weight. Aphid suppression of a calcium EF hand gene and OPR1 was lost when salt-sensitive soybean plants were salt stressed and when salt-tolerant plants were subjected to all three stressors. The relative levels of SMV in aphid-infested soybeans were increased by salt stress in the salt-sensitive cultivar, whereas SMV levels decreased in the salt-tolerant cultivar. Static headspace collection of volatile organic compounds revealed that salt stress and SMV infection had suppressive activities on aphid-induced terpenes. These results suggest that although salt stress has a negative impact on aphid population size, the changes in volatiles and SMV levels could alter the incidence of SMV in salt-stressed fields.

Keywords

Plant Agriculture Insect 

Notes

Acknowledgements

We wish to thank Lacy D. Nelson for her technical assistance and Kate Martin for critically reviewing the manuscript. We also thank Matt O’Neal from Iowa State University for kindly providing soybean aphids to start our colony. The authors also thank two anonymous reviewers for their helpful comments on improving the manuscript. Support was provided by the Arkansas Soybean Promotion Board, the Arkansas Center for Plant Powered Production, and the USDA National Institute of Food and Agriculture, Hatch Project 1011326.

Supplementary material

11829_2017_9590_MOESM1_ESM.docx (25 kb)
Supplementary material 1 (DOCX 24 KB)

References

  1. Abel GH (1969) Inheritance of the capacity for chloride inclusion and chloride exclusion by soybeans. Crop Sci 9:697.  https://doi.org/10.2135/cropsci1969.0011183X000900060006x CrossRefGoogle Scholar
  2. Baldwin IT, Halitschke R, Paschold A et al (2006) Volatile signaling in plant-plant interactions: “Talking Trees” in the genomics era. Science 311:812–815.  https://doi.org/10.1126/science.1118446 CrossRefPubMedGoogle Scholar
  3. Benjamins R, Ampudia CSG, Hooykaas PJJ, Offringa R (2003) PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol 132:1623–1630.  https://doi.org/10.1104/pp.103.019943 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bleeker PM, Diergaarde PJ, Ament K et al (2009) The role of specific tomato volatiles in tomato-whitefly interaction. Plant Physiol 151:925–935.  https://doi.org/10.1104/pp.109.142661 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bol JF, Linthorst HJM, Cornelissen BJC (1990) Plant pathogenesis-related proteins induced by virus infection. Ann Rev Phytopathol 28:113–138.  https://doi.org/10.1146/annurev.py.28.090190.000553 CrossRefGoogle Scholar
  6. Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030.  https://doi.org/10.1104/pp.126.3.1024 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bruce TJA, Matthes MC, Chamberlain K et al (2008) cis-Jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids. Proc Natl Acad Sci USA 105:4553–4558.  https://doi.org/10.1073/pnas.0710305105 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Carelli M, Biazzi E, Panara F et al (2011) Medicago truncatula CYP716A12 is a multifunctional oxidase involved in the biosynthesis of hemolytic saponins. Plant Cell 23:3070–3081.  https://doi.org/10.1105/tpc.111.087312 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chapple C (1998) Molecular-genetic analysis of plant cytochrome P450-dependent monooxygenases. Ann Rev Plant Physiol 49:311–343.  https://doi.org/10.1146/annurev.arplant.49.1.311 CrossRefGoogle Scholar
  10. Dáder B, Then C, Berthelot E et al (2017) Insect transmission of plant viruses: multilayered interactions optimize viral propagation. Insect Sci.  https://doi.org/10.1111/1744-7917.12470 Google Scholar
  11. Delp G, Gradin T, Åhman I, Jonsson LMV (2009) Microarray analysis of the interaction between the aphid Rhopalosiphum padi and host plants reveals both differences and similarities between susceptible and partially resistant barley lines. Mol Genet Genomics 281:233–248.  https://doi.org/10.1007/s00438-008-0409-3 CrossRefPubMedGoogle Scholar
  12. Devoto A, Turner JG (2003) Regulation of jasmonate-mediated plant responses in Arabidopsis. Ann Bot 92:329–337.  https://doi.org/10.1093/aob/mcg151 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dicke M, Beek TAV, Posthumus MA et al (1990) Isolation and identification of volatile kairomone that affects acarine predatorprey interactions involvement of host plant in its production. J Chem Ecol 16:381–396.  https://doi.org/10.1007/BF01021772 CrossRefPubMedGoogle Scholar
  14. Donaldson JR, Gratton C (2007) Antagonistic effects of soybean viruses on soybean aphid performance. Environ Entomol 36:918–925.  https://doi.org/10.1603/0046-225X(2007)36[918:AEOSVO]2.0.CO;2 CrossRefPubMedGoogle Scholar
  15. Dong W, Wang M, Xu F et al (2013) Wheat oxophytodienoate reductase gene TaOPR1 confers salinity tolerance via enhancement of abscisic acid signaling and reactive oxygen species scavenging. Plant Physiol 161:1217–1228.  https://doi.org/10.1104/pp.112.211854 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Eigenbrode SD, Bosque-Pérez N, Davis TS (2018) Insect-borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annu Rev Entomol.  https://doi.org/10.1146/annurev-ento-020117-043119 PubMedGoogle Scholar
  17. Farag MA, Fokar M, Abd H et al (2005) (Z)-3-Hexenol induces defense genes and downstream metabolites in maize. Planta 220:900–909.  https://doi.org/10.1007/s00425-004-1404-5 CrossRefPubMedGoogle Scholar
  18. Feng H, Wang X, Sun Y et al (2011) Cloning and characterization of a calcium binding EF-hand protein gene TaCab1 from wheat and its expression in response to Puccinia striiformis f. sp. tritici and abiotic stresses. Mol Biol Rep 38:3857–3866.  https://doi.org/10.1007/s11033-010-0501-8 CrossRefPubMedGoogle Scholar
  19. García-Marcos A, Pacheco R, Martiáñez J et al (2009) Transcriptional changes and oxidative stress associated with the synergistic interaction between Potato virus X and Potato virus Y and their relationship with symptom expression. Mol Plant Microbe Interact 22:1431–1444.  https://doi.org/10.1094/MPMI-22-11-1431 CrossRefPubMedGoogle Scholar
  20. Guan R, Qu Y, Guo Y et al (2014) Salinity tolerance in soybean is modulated by natural variation in GmSALT3. Plant J 80:937–950.  https://doi.org/10.1111/tpj.12695 CrossRefPubMedGoogle Scholar
  21. Guttikonda SK, Trupti J, Bisht NC et al (2010) Whole genome co-expression analysis of soybean cytochrome P450 genes identifies nodulation-specific P450 monooxygenases. BMC Plant Biol 10:243.  https://doi.org/10.1186/1471-2229-10-243 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hattori M, Nakamura M, Komatsu S et al (2012) Molecular cloning of a novel calcium-binding protein in the secreted saliva of the green rice leafhopper Nephotettix cincticeps. Insect Biochem Mol 42:1–9.  https://doi.org/10.1016/j.ibmb.2011.10.001 CrossRefGoogle Scholar
  23. Heil M, Bueno JCS (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472.  https://doi.org/10.1073/pnas.0610266104 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hernández JA, Rubio M, Olmos E et al (2004) Oxidative stress induced by long-term Plum pox virus infection in peach (Prunus persica). Physiol Plant 122:486–495.  https://doi.org/10.1111/j.1399-3054.2004.00431.x CrossRefGoogle Scholar
  25. Hill JH, Alleman R, Hogg DB, Grau CR (2001) First report of transmission of Soybean mosaic virus and Alfalfa mosaic virus by Aphis glycines in the New World. Plant Dis 85:561–561.  https://doi.org/10.1094/PDIS.2001.85.5.561C CrossRefGoogle Scholar
  26. Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184.  https://doi.org/10.1016/j.tplants.2010.01.006 CrossRefPubMedGoogle Scholar
  27. Ingwell LL, Eigenbrode SD, Bosque-Pérez NA (2012) Plant viruses alter insect behavior to enhance their spread. Sci Rep.  https://doi.org/10.1038/srep00578 PubMedPubMedCentralGoogle Scholar
  28. Jossey S, Hobbs HA, Domier LL (2013) Role of Soybean mosaic virus-encoded proteins in seed and aphid transmission in soybean. Phytopathology 103:941–948.  https://doi.org/10.1094/PHYTO-09-12-0248-R CrossRefPubMedGoogle Scholar
  29. Jovel J, Walker M, Sanfaçon H (2011) Salicylic acid-dependent restriction of Tomato ringspot virus spread in tobacco is accompanied by a hypersensitive response, local RNA silencing, and moderate systemic resistance. Mol Plant Microbe Interact 24:706–718.  https://doi.org/10.1094/MPMI-09-10-0224 CrossRefPubMedGoogle Scholar
  30. Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2005) Volatile C6-aldehydes and allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46:1093–1102.  https://doi.org/10.1093/pcp/pci122 CrossRefPubMedGoogle Scholar
  31. Koning G, TeKrony DM, Ghabrial SA, Pfeiffer TW (2002) Soybean mosaic virus (SMV) and the SMV resistance gene (Rsv(1): influence on Phomopsis spp. seed infection in an aphid free environment. Crop Sci 42:178–185.  https://doi.org/10.2135/cropsci2002.0178 CrossRefPubMedGoogle Scholar
  32. Konishi H, Noda H, Tamura Y, Hattori M (2009) Proteomic analysis of the salivary glands of the rice brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae). Appl Entomol Zool 44:525–534.  https://doi.org/10.1303/aez.2009.525 CrossRefGoogle Scholar
  33. Kuśnierczyk A, Winge P, Midelfart H et al (2007) Transcriptional responses of Arabidopsis thaliana ecotypes with different glucosinolate profiles after attack by polyphagous Myzus persicae and oligophagous Brevicoryne brassicae. J Exp Bot 58:2537–2552.  https://doi.org/10.1093/jxb/erm043 CrossRefPubMedGoogle Scholar
  34. Kuśnierczyk A, Tran DH, Winge P et al (2011) Testing the importance of jasmonate signalling in induction of plant defenses upon cabbage aphid (Brevicoryne brassicae) attack. BMC Genomics 12:423.  https://doi.org/10.1186/1471-2164-12-423 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Laney AG (2014). The phenotypic effects and transcript response of salt stress, the impact of viral infection on salt stress symptoms, and the effect of salt stress on soybean virus vector activity in soybean varieties that vary in chloride uptake. Dissertation, University of ArkansasGoogle Scholar
  36. Le DT, Aldrich DL, Valliyodan B 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.  https://doi.org/10.1371/journal.pone.0046487 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Li Y, Zou J, Li M et al (2008) Soybean defense responses to the soybean aphid. New Phytol 179:185–195.  https://doi.org/10.1111/j.1469-8137.2008.02443.x CrossRefPubMedGoogle Scholar
  38. Li D, Chen P, Alloatti J, Shi A, Chen YF (2010) Identification of new alleles for resistance to Soybean mosaic virus in soybean. Crop Sci 50:649–655.  https://doi.org/10.2135/cropsci2009.06.0302 CrossRefGoogle Scholar
  39. Liu J, Zhu J-K (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945.  https://doi.org/10.1126/science.280.5371.1943 CrossRefPubMedGoogle Scholar
  40. Liu C-J, Huhman D, Sumner LW, Dixon RA (2003) Regiospecific hydroxylation of isoflavones by cytochrome P450 81E enzymes from Medicago truncatula. Plant J 36:471–484.  https://doi.org/10.1046/j.1365-313X.2003.01893.x CrossRefPubMedGoogle Scholar
  41. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods 25:402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefPubMedGoogle Scholar
  42. Matsui K, Sugimoto K, Mano J et al (2012) Differential metabolisms of green leaf volatiles in injured and intact parts of a wounded leaf meet distinct ecophysiological requirements. PLoS ONE 7:e36433.  https://doi.org/10.1371/journal.pone.0036433 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Matthes MC, Bruce TJA, Ton J et al (2010) The transcriptome of cis-jasmone-induced resistance in Arabidopsis thaliana and its role in indirect defence. Planta 232:1163–1180.  https://doi.org/10.1007/s00425-010-1244-4 CrossRefPubMedGoogle Scholar
  44. McCormack E, Tsai Y-C, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389.  https://doi.org/10.1016/j.tplants.2005.07.001 CrossRefPubMedGoogle Scholar
  45. McWilliams DA, Berglund DR, Endres GJ (1999) Soybean growth and management quick guide. NDSU Extension Service A-1174Google Scholar
  46. Medina-Ortega KJ, Bosque-Pérez NA, Ngumbi E et al (2009) Rhopalosiphum padi (Hemiptera: Aphididae) responses to volatile cues from Barley yellow dwarf virus-infected wheat. Environ Entomol 38:836–845.  https://doi.org/10.1603/022.038.0337 CrossRefPubMedGoogle Scholar
  47. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498.  https://doi.org/10.1016/j.tplants.2004.08.009 CrossRefPubMedGoogle Scholar
  48. Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573.  htpps://doi.org/10.1038/31219
  49. Moraes MCB, Laumann RA, Pareja M et al (2009) Attraction of the stink bug egg parasitoid Telenomus podisi to defence signals from soybean activated by treatment with cis-jasmone. Entomol Exp Appl 131:178–188.  https://doi.org/10.1111/j.1570-7458.2009.00836.x CrossRefGoogle Scholar
  50. Müssig C, Biesgen C, Lisso J et al (2000) A novel stress-inducible 12-oxophytodienoate reductase from Arabidopsis thaliana provides a potential link between Brassinosteroid-action and Jasmonic-acid synthesis. J Plant Physiol 157:143–152.  https://doi.org/10.1016/S0176-1617(00)80184-4 CrossRefGoogle Scholar
  51. Nalam VJ, Keeretaweep J, Sarowar S, Shah J (2012) Root-derived oxylipins promote green peach aphid performance on Arabidopsis Foliage. Plant Cell 24:1643–1653.  https://doi.org/10.1105/tpc.111.094110 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Naoumkina MA, Modolo LV, Huhman DV et al (2010) Genomic and co-expression analyses predict multiple genes involved in triterpene saponin biosynthesis in Medicago truncatula. Plant Cell 22:850–866.  https://doi.org/10.1105/tpc.109.073270 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Naur P, Petersen BL, Mikkelsen MD et al (2003) CYP83A1 and CYP83B1, two non-redundant cytochrome P450 enzymes metabolizing oximes in the biosynthesis of glucosinolates in Arabidopsis. Plant Physiol 133:63–72.  https://doi.org/10.1104/pp.102.019240 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Ngumbi E, Eigenbrode SD, Bosque-Pérez NA et al (2007) Myzus persicae is arrested more by blends than by individual compounds elevated in headspace of Potato leaf roll virus-infected potato. J Chem Ecol 33:1733–1747.  https://doi.org/10.1007/s10886-007-9340-z CrossRefPubMedGoogle Scholar
  55. Pare PW, Tumlinson JH (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114:1161–1167.  https://doi.org/10.1104/pp.114.4.1161 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Paré PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–332.  https://doi.org/10.1104/pp.121.2.325 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Pareja M, Moraes MCB, Clark SJ et al (2007) Response of the aphid parasitoid Aphidius funebris to volatiles from undamaged and aphid-infested Centaurea nigra. J Chem Ecol 33:695–710.  https://doi.org/10.1007/s10886-007-9260-y CrossRefPubMedGoogle Scholar
  58. Peñaflor MFGV., Mauck KE, Alves KJ et al (2016) Effects of single and mixed infections of Bean pod mottle virus and Soybean mosaic virus on host-plant chemistry and host–vector interactions. Funct Ecol 30:1648–1659.  https://doi.org/10.1111/1365-2435.12649 CrossRefGoogle Scholar
  59. Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Bio 5:237–243.  https://doi.org/10.1016/S1369-5266(02)00251-0 CrossRefGoogle Scholar
  60. Qi X, Li M-W, Xie M et al (2014) Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nat Commun 5:4340.  https://doi.org/10.1038/ncomms5340 PubMedPubMedCentralGoogle Scholar
  61. Ragsdale DW, Voegtlin DJ, O’Neil RJ (2004) Soybean aphid biology in North America. Ann Entomol Soc Am 97:204–208.  https://doi.org/10.1603/0013-8746(2004)097[0204:SABINA]2.0.CO;2 CrossRefGoogle Scholar
  62. 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.  http://doi.org/10.1146/annurev-ento-120709-144755
  63. Ramachandran R, Norris DM, Phillips JK, Phillips TW (1991) Volatiles mediating plant-herbivore-natural enemy interactions: soybean looper frass volatiles, 3-octanone and guaiacol, as kairomones for the parasitoid Microplitis demolitor. J Agric Food Chem 39:2310–2317.  https://doi.org/10.1021/jf00012a044 CrossRefGoogle Scholar
  64. Rawlins T, Tompkins C (1936) Studies on the effect of carborundum as an abrasive in plant virus inoculations. Phytopathology 26:578–587Google Scholar
  65. Sasaki Y, Asamizu E, Shibata D et al (2001) Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA microarray: self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res 8:153–161.  https://doi.org/10.1093/dnares/8.4.153 CrossRefPubMedGoogle Scholar
  66. Schaller F, Biesgen C, Müssig C et al (2000) 12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis. Planta 210:979–984.  https://doi.org/10.1007/s004250050706 CrossRefPubMedGoogle Scholar
  67. Schuler MA (1996) The role of cytochrome P450 monooxygenases in plant-insect interactions. Plant Physiol 112:1411–1419CrossRefPubMedPubMedCentralGoogle Scholar
  68. Selig P, Keough S, Nalam VJ et al (2016) Jasmonate-dependent plant defenses mediate soybean thrips and soybean aphid performance on soybean. Arthropod-Plant Interact 10:273–282.  https://doi.org/10.1007/s11829-016-9437-9 CrossRefGoogle Scholar
  69. Shen J, Tieman D, Jones JB et al (2014) A 13-lipoxygenase, TomloxC, is essential for synthesis of C5 flavour volatiles in tomato. J Exp Bot 65:419–428.  https://doi.org/10.1093/jxb/ert382 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Smith CM, Boyko EV (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol Exp Appl 122:1–16.  https://doi.org/10.1111/j.1570-7458.2006.00503.x CrossRefGoogle Scholar
  71. 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.  https://doi.org/10.1094/MPMI-05-12-0124-FI CrossRefPubMedGoogle Scholar
  72. Tanji KK (2002) Agricultural drainage water management in arid and semi-arid areas. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  73. Ton J, D’Alessandro M, Jourdie V et al (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26.  https://doi.org/10.1111/j.1365-313X.2006.02935.x CrossRefPubMedGoogle Scholar
  74. Turlings TC, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253.  https://doi.org/10.1126/science.250.4985.1251 CrossRefPubMedGoogle Scholar
  75. Turlings TC, Loughrin JH, McCall PJ et al (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci USA 92:4169–4174CrossRefPubMedPubMedCentralGoogle Scholar
  76. Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:S153–S164.  https://doi.org/10.1105/tpc.000679 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Tzanetakis IE, Postman JD, Martin RR (2007) Identification, detection and transmission of a new vitivirus from Mentha. Arch Virol 152:2027–2033.  https://doi.org/10.1007/s00705-007-1030-1 CrossRefPubMedGoogle Scholar
  78. Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485.  https://doi.org/10.1016/j.pbi.2009.04.001 CrossRefPubMedGoogle Scholar
  79. Van Den Boom CEM, Beek TAV, Posthumus MA et al (2004) Qualitative and quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from various families. J Chem Ecol 30:69–89.  https://doi.org/10.1023/B:JOEC.0000013183.72915.99 CrossRefPubMedGoogle Scholar
  80. Venette RC, Ragsdale DW (2004) Assessing the invasion by soybean aphid (Homoptera: Aphididae): where will it end? Ann Entomol Soc Am 97:219–226.  https://doi.org/10.1603/0013-8746(2004)097[0219:ATIBSA]2.0.CO;2 CrossRefGoogle Scholar
  81. Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291.  https://doi.org/10.1038/nchembio.158 CrossRefPubMedGoogle Scholar
  82. Voelckel C, Weisser WW, Baldwin IT (2004) An analysis of plant-aphid interactions by different microarray hybridization strategies. Mol Ecol 13:3187–3195.  https://doi.org/10.1111/j.1365-294X.2004.02297.x CrossRefPubMedGoogle Scholar
  83. Wang RY, Ghabrial SA (2002) Effect of aphid behavior on efficiency of transmission of Soybean mosaic virus by the soybean-colonizing aphid, Aphis glycines. Plant Dis 86:1260–1264.  https://doi.org/10.1094/PDIS.2002.86.11.1260 CrossRefGoogle Scholar
  84. Wang X, Goregaoker SP, Culver JN (2009) Interaction of the Tobacco mosaic virus replicase protein with a NAC domain transcription factor is associated with the suppression of systemic host defenses. J Virol 83:9720–9730.  https://doi.org/10.1128/JVI.00941-09 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Wei J-R, Yang Z-Q, Hao H-L, Du J-W (2008) (R)-(+)-limonene, kairomone for Dastarcus helophoroides, a natural enemy of longhorned beetles. Agric For Entomol 10:323–330.  https://doi.org/10.1111/j.1461-9563.2008.00384.x CrossRefGoogle Scholar
  86. Whitman DW, Eller FJ (1990) Parasitic wasps orient to green leaf volatiles. Chemoecology 1:69–76.  https://doi.org/10.1007/BF01325231 CrossRefGoogle Scholar
  87. Will T, Tjallingii WF, Thönnessen A, Bel AJE van (2007) Molecular sabotage of plant defense by aphid saliva. Proc Natl Acad Sci USA 104:10536–10541.  https://doi.org/10.1073/pnas.0703535104 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8:505–512.  https://doi.org/10.1016/j.tplants.2003.09.004 CrossRefPubMedGoogle Scholar
  89. Zhu J-K (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124:941–948.  https://doi.org/10.1104/pp.124.3.941 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Zhu J, Park K-C (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J Chem Ecol 31:1733–1746.  https://doi.org/10.1007/s10886-005-5923-8 CrossRefPubMedGoogle Scholar
  91. Zhuang BC, Xu B, Liao L (1993) Change of superoxide dismutase, peroxidase and storage protein in soybean leaves after inoculation with Soybean mosaic virus. Acta Phytopathol Sin 23:261–265Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Plant Pathology, Division of AgricultureUniversity of ArkansasFayettevilleUSA
  2. 2.Department of Crop, Soil, and Environmental Sciences, Division of AgricultureUniversity of ArkansasFayettevilleUSA
  3. 3.Department of Entomology and Plant PathologyNorth Carolina State UniversityRaleighUSA
  4. 4.Division of Plant Sciences, Fisher Delta Research CenterUniversity of MissouriPortagevilleUSA

Personalised recommendations