Advertisement

Maize Iranian mosaic virus (family Rhabdoviridae) improves biological traits of its vector Laodelphax striatellus

  • Pedram Moeini
  • Alireza AfsharifarEmail author
  • Keramatollah Izadpanah
  • Seyed Ebrahim Sadeghi
  • Sanford D. Eigenbrode
Original Article
  • 41 Downloads

Abstract

Plant viruses can alter the behavior or performance of their arthropod vectors, either indirectly (through effects of virus infection on the host plant) or directly (from virus acquisition by the vector). Given the diversity of plant viruses and their arthropod vectors, the effects for any specific system are not possible to predict. Here, we present experimental evidence that acquisition of maize Iranian mosaic virus (MIMV, genus Nucleorhabdovirus, family Rhabdoviridae) modifies the biological traits of its insect vector, the small brown planthopper (SBPH) Laodelphax striatellus. MIMV is an economically important virus of maize and several other grass species. It is transmitted by SBPHs in a persistent-propagative manner. We evaluated the effects of MIMV acquisition by SBPH on its life history when reared on healthy barley plants (Hordeum vulgare). We conclude that 1) MIMV acquisition by SBPHs increases female fecundity, duration of the nymph stage, adult longevity, and survival of SBPHs, (2) the mortality rate and female-to-male sex ratio are reduced in MIMV-infected planthoppers, and (3) MIMV infection increases the concentration of some biochemical components of the infected plants, including carbohydrates, some amino acids, and total protein, which might influence the life traits of its insect vector. The results indicate the potential of MIMV to improve the ecological fitness of its vector, SBPH, through direct or indirect effects, with the potential to increase the spread of the virus.

Notes

Acknowledgments

The authors would like to thank the Plant Virology Research Center for supporting this research in the College of Agriculture, Shiraz University, Shiraz-Iran.

Compliance with ethical standards

All authors contributed critically to the drafts and gave final approval for publication. This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Eigenbrode SD, Bosque-Pérez NA, Davis TS (2018) Insect-borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annu Rev Entomol 63:169–1911PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Matsuura S, Hoshino S (2009) Effect of tomato yellow leaf curl disease on reproduction of Bemisia tabaci Q biotype (Hemiptera:Aleyrodidae) on tomato plants. Appl Entomol Zool 44:143–148CrossRefGoogle Scholar
  3. 3.
    Maris PC, Joosten NN, Goldbach RW, Peters D (2004) Tomato spotted wilt virus infection improves host suitability for its vector Frankliniella occidentalis. Phytopathology 94:706–711PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Belliure B, Janssen A, Maris PC, Peters D, Sabelis MW (2005) Herbivore arthropods benefit from vectoring plant viruses. Ecol Lett 8:70–79CrossRefGoogle Scholar
  5. 5.
    Rubinstein G, Czosnek H (1997) Long-term association of Tomato yellow leaf curl virus with its whitefly vector Bemisia tabaci: effect on the insect transmission capacity, longevity and fecundity. J Gen Virol 78:2683–2689PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Fereres A, Moreno A (2009) Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Res 141:158–168PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Mauck KE, Bosque-Pérez NA, Eigenbrode SD, De Moraes CM, Mescher MC (2012) Transmission mechanisms shape pathogen effects on host–vector interactions: evidence from plant viruses. Funct Ecol 26:1162–1175CrossRefGoogle Scholar
  8. 8.
    Mauck KE, De Moraes CM, Mescher MC (2016) Effects of pathogens on sensory-mediated interactions between plants and insect vectors. Curr Opin Plant Biol 32:53–61PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Jiu M, Zhou XP, Tong L, Xu J, Yang X, Wan FH, Liu SS (2007) Vector-virus mutualism accelerates population increase of an invasive whitefly. PloS One 2:e182PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Barandoc-Alviar K, Badillo-Vargas IE, Whitfield AE (2016) Interactions between insect vectors and propagative plant viruses. In: Czosnek H, Ghanim M (eds) Management of insect pests to agriculture. Springer, Cham, pp 133–180CrossRefGoogle Scholar
  11. 11.
    Chen Y, Lu C, Li M, Wu W, Zhou G, Wei T (2016) Adverse effects of Rice gall dwarf virus upon its insect vector Reciliadorsalis (Hemiptera:Cicadellidae). Plant Dis 100:784–790PubMedCrossRefGoogle Scholar
  12. 12.
    Ingwell LL, Eigenbrode SD, Bosque-Pérez NA (2012) Plant viruses alter insect behavior to enhance their spread. Sci Rep 2:578PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Deangelis JD, Sether D, Rossignol P (1993) Survival, development, and reproduction in western flower thrips (Thysanoptera:Thripidae) exposed to Impatiens necrotic spot virus. Environ Entomol 22:1308–1312CrossRefGoogle Scholar
  14. 14.
    Tu Z, Ling B, Xu D, Zhang M, Zhou G (2013) Effects of Southern rice black-streaked dwarf virus on the development and fecundity of its vector, Sogatella furcifera. Virol J 10:145PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Hogenhout SA, Ammar ED, Whitfield AE, Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Ammar ED, Tsai CW, Whitfield AE, Redinbaugh MG, Hogenhout SA (2009) Cellular and molecular aspects of rhabdovirus interactions with insect and plant hosts. Annu Rev Entomol 54:447–468CrossRefGoogle Scholar
  17. 17.
    Li S, Wang S, Wang X, Li X, Zi J, Ge S, Wong SM (2015) Rice stripe virus affects the viability of its vector offspring by changing developmental gene expression in embryos. Sci Rep 5:7883PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Bosque-Pérez NA, Eigenbrode SD (2011) The influence of virus-induced changes in plants on aphid vectors: insights from luteovirus pathosystems. Virus Res 159:201–205PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Czosnek H, Ghanim M (2012) Back to basics: are begomoviruses whitefly pathogens? J Integr Agric 11:225–234CrossRefGoogle Scholar
  20. 20.
    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 USA 107:3600–3605PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    McMenemy LS, Hartley SE, MacFarlane SA, Karley AJ, Shepherd T, Johnson SN (2012) Raspberry viruses manipulate the behaviour of their insect vectors. Entomol Exp Appl 144:56–68CrossRefGoogle Scholar
  22. 22.
    Oluwafemi S, Bruce TJ, Pickett JA, Ton J, Birkett MA (2011) Behavioral responses of the leafhopper, Cicadulina storeyi China, a major vector of Maize streak virus, to volatile cues from intact and leafhopper-damaged maize. J Chem Ecol 37:40–48PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Xu H, He X, Zheng X, Yang Y, Tian J, Lu Z (2014) Southern rice black-streaked dwarf virus (SRBSDV) directly affects the feeding and reproduction behavior of its vector, Sogatella furcifera (Horváth) (Hemiptera:Delphacidae). Virol J 11:55PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Eigenbrode SD, Ding H, Shiel P, Berger PH (2002) Volatiles from potato plants infected with Potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc R Soc Lond Biol 269:455–460CrossRefGoogle Scholar
  25. 25.
    Mauck KE, De Moraes CM, Mescher MC (2014) Biochemical and physiological mechanisms underlying effects of Cucumber mosaic virus on host-plant traits that mediate transmission by aphid vectors. Plant Cell Environ 37:1427–1439PubMedCrossRefGoogle Scholar
  26. 26.
    Xu HX, He XC, Zheng XS, Yang YJ, Lu ZX (2014) Influence of Rice black streaked dwarf virus on the ecological fitness of non-vector planthopper Nilaparvata lugens (Hemiptera: Delphacidae). Insect Sci 21:507–514PubMedCrossRefGoogle Scholar
  27. 27.
    Smith CM, Gedling CR, Wiebe KF, Cassone BJ (2017) A sweet story: Bean pod mottle virus transmission dynamics by Mexican bean beetles (Epilachna varivestis). Genome Biol Evol 9:714–725PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    Zografou E, Tsiropoulos G, Margaritis L (1998) Survival, fecundity and fertility of Bactrocera oleae, as affected by amino acid analogues. Entomol Exp Appl 87:125–132CrossRefGoogle Scholar
  29. 29.
    Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844PubMedCrossRefGoogle Scholar
  30. 30.
    Le Gall M, Behmer ST (2014) Effects of protein and carbohydrate on an insect herbivore: the vista from a fitness landscape. Integr Comp Biol 54:942–954PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Roeder KA, Behmer ST (2014) Lifetime consequences of food protein-carbohydrate content for an insect herbivore. Funct Ecol 28:1135–1143CrossRefGoogle Scholar
  32. 32.
    Izadpanah K, Parvin S (1979) Occurrence of Maize mosaic virus in corn fields around Shiraz. Iran J Plant Pathol 15:53–54Google Scholar
  33. 33.
    Massah A, Izadpanah K, Afsharifar A, Winter S (2008) Analysis of nucleotide sequence of Iranian maize mosaic virus confirms its identity as a distinct nucleorhabdovirus. Arch Virol 153:1041–1047PubMedCrossRefGoogle Scholar
  34. 34.
    Izadpanah K, Ahmadi AA, Parvin S, Jafari SA (1983) Transmission, particle size and additional hosts of the rhabdovirus causing maize mosaic in Shiraz, Iran. J Phytopathol 107:283–288CrossRefGoogle Scholar
  35. 35.
    Jackson AO, Dietzgen RG, Goodin MM, Bragg JN, Deng M (2005) Biology of plant rhabdoviruses. Annu Rev Phytopathol 43:623–660PubMedCrossRefGoogle Scholar
  36. 36.
    Redinbaugh MG, Hogenhout SA (2005) Plant rhabdoviruses. Curr Top Microbiol 292:143–163Google Scholar
  37. 37.
    Lapierre H, Signoret PA (eds) (2004) Viruses and virus diseases of Poaceae (Gramineae). Technology and Engineering, Institute National de la Recherche Agronomique, ParisGoogle Scholar
  38. 38.
    Jeong TW, Kim BR, Han GS, Kang DW, Jeong IY, Lim HS, Kim JS (2012) Evaluation of pesticide treatment for control of Rice stripe virus after mass migration of small brown planthoppers. Res Plant Dis 18:245–249CrossRefGoogle Scholar
  39. 39.
    Otuka A (2013) Migration of rice planthoppers and their vectored re-emerging and novel rice viruses in East Asia. Front Microbiol 4:309PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Massah A (2005) Sequencing, Taxonomy and certain aspects of virus-vector relationship of Iranian Maize Mosaic Rhabdovirus. Doctoral thesis, Shiraz University, p 75Google Scholar
  41. 41.
    Sun JT, Wang MM, Zhang YK, Chapuis MP, Jiang XY, Hu G, Hong XY (2015) Evidence for high dispersal ability and mito-nuclear discordance in the small brown planthopper, Laodelphax striatellus. Sci Rep 5:8045PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Hilario E, Mackay JF (2007) Protocols for nucleic acid analysis by nonradioactive probes. Methods in molecular biology, vol 353. Humana PressGoogle Scholar
  43. 43.
    Altschul SF, Gish W, Miller W, Myers EW, Lipman D (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Izadpanah K (1989) Purification and serology of the Iranian maize mosaic rhabdovirus. J Phytopathol 126:43–50CrossRefGoogle Scholar
  45. 45.
    Hortamani M, Massah A, Izadpanah K (2018) Maize Iranian mosaic virus shows a descending transcript accumulation order in plant and insect hosts. Archiv Virol 163:887–893CrossRefGoogle Scholar
  46. 46.
    Meyer MD, Terry LA (2008) Development of a rapid method for the sequential extraction and subsequent quantification of fatty acids and sugars from avocado mesocarp tissue. J Agric Food Chem 56:7439–7445PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    SAS Institute Inc (2004) SAS/STAT® 9.1 user’s Guide. SAS Institute Inc, CaryGoogle Scholar
  49. 49.
    Dáder B, Then C, Berthelot E, Ducousso M, Ng JC, Drucker M (2017) Insect transmission of plant viruses: multilayered interactions optimize viral propagation. Insect Sci 24:929–946PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Barandoc-Alviar K, Ramirez GM, Rotenberg D, Whitfield AE (2016) Analysis of acquisition and titer of maize mosaic rhabdovirus in its vector, Peregrinus maidis (Hemiptera: Delphacidae). J Insect Sci 16:1–8CrossRefGoogle Scholar
  51. 51.
    Martin KM, Barandoc-Alviar K, Schneweis DJ, Stewart CL, Rotenberg D, Whitfield AE (2017) Transcriptomic response of the insect vector, Peregrinus maidis, to Maize mosaic rhabdovirus and identification of conserved responses to propagative viruses in hopper vectors. Virol 509:71–81CrossRefGoogle Scholar
  52. 52.
    Stout MJ, Thaler JS, Thomma BP (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu Rev Entomol 51:663–689PubMedCrossRefGoogle Scholar
  53. 53.
    Luan JB, Yao DM, Zhang T, Walling LL, Yang M, Wang YJ, Liu SS (2013) Suppression of terpenoid synthesis in plants by a virus promotes its mutualism with vectors. Ecol Lett 16:390–398PubMedCrossRefGoogle Scholar
  54. 54.
    Liu S, Ding Z, Zhang C, Yang B, Liu Z (2010) Gene knockdown by intro-thoracic injection of double-stranded RNA in the brown planthopper, Nilaparvata lugens. Insect Biochem Mol 40:666–671CrossRefGoogle Scholar
  55. 55.
    Yao J, Rotenberg D, Whitfield AE (2019) Delivery of maize mosaic virus to planthopper vectors by microinjection increases infection efficiency and facilitates functional genomics experiments in the vector. J Virol Methods 270:153–162PubMedCrossRefGoogle Scholar
  56. 56.
    Guo JY, Dong SZ, Yang XL, Cheng L, Wan FH, Liu SS, Ye GY (2012) Enhanced vitellogenesis in a whitefly via feeding on a begomovirus-infected plant. PLoS One 7:e43567PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Shrestha A, Srinivasan R, Riley DG, Culbreath AK (2012) Direct and indirect effects of a thrips-transmitted Tospovirus on the preference and fitness of its vector, Frankliniella fusca. Entomol Exp Appl 145:260–271CrossRefGoogle Scholar
  58. 58.
    Ding JH, Dou J (1990) Usage of free amino acid to brown planthopper, Nilaparvata lugens. Chin Bull Entomol 27:65–67Google Scholar
  59. 59.
    Koyama K, Mitsuhashi J (1975) Essential amino acids for the growth of the smaller brown planthopper, Laodelphax striatellus Fallen:Hemiptera:Delphacidae. Appl Entomol Zool 10:208–215CrossRefGoogle Scholar
  60. 60.
    Wilkinson TL, Douglas AE (2003) Phloem amino acids and the host plant range of the polyphagous aphid, Aphis fabae. Entomol Exp Appl 106:103–113CrossRefGoogle Scholar
  61. 61.
    Fu Q, Zhang Z, Hu C, Zhu Z, Lai F (2000) Effects of dietary amino acids on free amino acid pools in the body and honeydew of the brown planthopper, Nilaparvata lugens. Zhongguo Shuidao Kexue 15:298–302Google Scholar
  62. 62.
    Tauzin AS, Giardina T (2014) Sucrose and invertases, a part of the plant defense response to the biotic stresses. Front Plant Sci 5:293PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    De Bruyn L, Scheirs J, Verhagen R (2002) Nutrient stress, host plant quality and herbivore performance of a leaf-mining fly on grass. Oecologia 130:594–599PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Douglas AE (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57:747–754PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Yoshida K, Sanada-Morimura S, Huang SH, Tokuda M (2019) Influences of two coexisting endosymbionts, CI-inducing Wolbachia and male-killing Spiroplasma, on the performance of their host Laodelphax striatellus (Hemiptera: Delphacidae). Ecol Evol 9:8214–8224PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Plant Virology Research Center, College of AgricultureShiraz UniversityShirazIran
  2. 2.Department of Plant Protection, Faculty of AgricultureUniversity of TehranKarajIran
  3. 3.Department of Entomology, Plant Pathology and Nematology, College of Agricultural and Life SciencesUniversity of IdahoMoscowUSA

Personalised recommendations