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Journal of General Virology header logo Journal of General Virology

Volume 105, Issue 7

Beet curly top virus affects vector biology: the first transcriptome analysis of the beet leafhopper Open Access

Abstract

Curly top disease, caused by beet curly top virus (BCTV), is among the most serious viral diseases affecting sugar beets in western USA. The virus is exclusively transmitted by the beet leafhopper (BLH, ) in a circulative and non-propagative manner. Despite the growing knowledge on virus-vector interactions, our understanding of the molecular interactions between BCTV and BLH is hampered by limited information regarding the virus impact on the vector and the lack of genomic and transcriptomic resources for BLH. This study unveils the significant impact of BCTV on both the performance and transcriptome response of BLHs. Viruliferous BLHs had higher fecundity than non-viruliferous counterparts, which was evident by upregulation of differentially expressed transcripts (DETs) associated with development, viability and fertility of germline and embryos in viruliferous insects. Conversely, most DETs associated with muscle movement and locomotor activities were downregulated in viruliferous insects, implying potential behavioural modifications by BCTV. Additionally, a great proportion of DETs related to innate immunity and detoxification were upregulated in viruliferous insects. Viral infection also induced notable alterations in primary metabolisms, including energy metabolism, namely glucosidases, lipid digestion and transport, and protein degradation, along with other cellular functions, particularly in chromatin remodelling and DNA repair. This study represents the first comprehensive transcriptome analysis for BLH. The presented findings provide new insights into the multifaceted effects of viral infection on various biological processes in BLH, offering a foundation for future investigations into the complex virus-vector relationship and potential management strategies for curly top disease.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Circulifer tenellus , Curtovirus , fecundity , transcriptome and virus-vector interaction
Funding
This study was supported by the:
  • USDA-ARS Sustainable Sugar Beet Research Initiative (Award N/A)
    • Principle Award Recipient: PunyaNachappa
  • Western Sugar Cooperative Research Committee (Award N/A)
    • Principle Award Recipient: PunyaNachappa
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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References

  1. Panella L, Kaffka SR, Lewellen RT, McGrath JM, Metzger MS et al. Sugarbeet. In Yield Gains in Major US Field Crops 2015 pp 357–395 [View Article]
     [Google Scholar]
  2. Bennett CW. The Curly Top Disease of Sugarbeet and Other Plants American Phytopathological Society; 1971 [View Article]
     [Google Scholar]
  3. Giladi Y, Hadad L, Luria N, Cranshaw W, Lachman O et al. First report of beet curly top virus infecting Cannabis sativa in Western Colorado. Plant Dis 2020; 104:999 [View Article]
     [Google Scholar]
  4. Harrison BD. Advances in geminivirus research. Annu Rev Phytopathol 1985; 23:55–82 [View Article]
     [Google Scholar]
  5. Strausbaugh CA, Eujayl IA, Wintermantel WM. Beet curly top virus strains associated with sugar beet in Idaho, Oregon, and a Western U.S. collection. Plant Dis 2017; 101:1373–1382 [View Article] [PubMed]
     [Google Scholar]
  6. Creamer R. Beet curly top virus transmission, epidemiology, and management. In Applied Plant Virology Academic Press; 2020 pp 521–527 [View Article]
     [Google Scholar]
  7. Chen L, Gilbertson RL. Chapter 17: Transmission of Curtoviruses (beet curly top virus) by the beet leafhopper (Circulifer tenellus). In Vector-Mediated Transmission of Plant Pathogens The American Phytopathological Society; pp 243–262 [View Article]
     [Google Scholar]
  8. Soto MJ, Gilbertson RL. Distribution and rate of movement of the curtovirus beet mild curly top virus (Family Geminiviridae) in the beet leafhopper. Phytopathology 2003; 93:478–484 [View Article] [PubMed]
     [Google Scholar]
  9. Bennett CW, Wallace HE. Relation of the curly top virus to the vector, Eutettix Tenellus. J Agric Res 1938; 56:31–51
     [Google Scholar]
  10. Freitag JH. Negative evidence on multiplication of curly-top virus in the beet leafhopper, Eutettix tenellus. Hilg 1936; 10:303–342 [View Article]
     [Google Scholar]
  11. Bennett CW. Acquisition and transmission of curly top virus by artificially fed beet leafhoppers. J Sugarbeet Res 1962; 11:637–648 [View Article]
     [Google Scholar]
  12. Gibson KE, Oliver W. Comparison of nymphal and adult beet leafhoppers as vectors of the virus of curly top1. J Econ Entomol 1970; 63:1321 [View Article]
     [Google Scholar]
  13. Eigenbrode SD, Bosque-Pérez NA, Davis TS. Insect-borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annu Rev Entomol 2018; 63:169–191 [View Article] [PubMed]
     [Google Scholar]
  14. Rajarapu SP, Ullman DE, Uzest M, Rotenberg D et al. Plant–virus–vector interactions. Virology 2021227–287 [View Article]
     [Google Scholar]
  15. Fereres A, Lister RM, Araya JE, Foster JE. Development and reproduction of the English grain aphid (Homoptera: Aphididae) on wheat cultivars infected with barley yellow dwarf virus. Environ Entomol 1989; 18:388–393 [View Article]
     [Google Scholar]
  16. Blua MJ, Perring TM, Madore MA. Plant virus-induced changes in aphid population development and temporal fluctuations in plant nutrients. J Chem Ecol 1994; 20:691–707 [View Article] [PubMed]
     [Google Scholar]
  17. Eigenbrode SD, Ding H, Shiel P, Berger PH. Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc R Soc Lond B 2002; 269:455–460 [View Article]
     [Google Scholar]
  18. Mauck KE, De Moraes CM, Mescher MC. Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proc Natl Acad Sci U S A 2010; 107:3600–3605 [View Article] [PubMed]
     [Google Scholar]
  19. Guo J-Y, Ye G-Y, Dong S-Z, Liu S-S. An invasive whitefly feeding on a virus-infected plant increased its egg production and realized fecundity. PLoS One 2010; 5:e11713 [View Article] [PubMed]
     [Google Scholar]
  20. Maris PC, Joosten NN, Goldbach RW, Peters D. Tomato spotted wilt virus infection improves host suitability for its vector Frankliniella occidentalis. Phytopathology 2004; 94:706–711 [View Article] [PubMed]
     [Google Scholar]
  21. Belliure B, Janssen A, Maris PC, Peters D, Sabelis MW. Herbivore arthropods benefit from vectoring plant viruses. Ecol Lett 2005; 8:70–79 [View Article]
     [Google Scholar]
  22. Abe H, Tomitaka Y, Shimoda T, Seo S, Sakurai T et al. Antagonistic plant defense system regulated by phytohormones assists interactions among vector insect, thrips and a tospovirus. Plant Cell Physiol 2012; 53:204–212 [View Article] [PubMed]
     [Google Scholar]
  23. Nachappa P, Challacombe J, Margolies DC, Nechols JR, Whitfield AE et al. Tomato spotted wilt virus benefits its thrips vector by modulating metabolic and plant defense pathways in tomato. Front Plant Sci 2020; 11:575564 [View Article]
     [Google Scholar]
  24. Severin HHP. Longevity, or life histories, of leafhopper species on virus-infected and on healthy plants. Hilg 1946; 17:121–137 [View Article]
     [Google Scholar]
  25. Lee H, Stephanus AP, Fowles TM, Wintermantel WM, Trumble JT et al. Insect vector manipulation by a plant virus and simulation modeling of its potential impact on crop infection. Sci Rep 2022; 12:8429 [View Article]
     [Google Scholar]
  26. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018; 34:i884–i890 [View Article] [PubMed]
     [Google Scholar]
  27. Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 2016; 11:1650–1667 [View Article] [PubMed]
     [Google Scholar]
  28. Smith-Unna R, Boursnell C, Patro R, Hibberd JM, Kelly S. TransRate: reference-free quality assessment of de novo transcriptome assemblies. Genome Res 2016; 26:1134–1144 [View Article] [PubMed]
     [Google Scholar]
  29. Manni M, Berkeley MR, Seppey M, Zdobnov EM. BUSCO: assessing genomic data quality and beyond. Curr Protoc 2021; 1:e323 [View Article] [PubMed]
     [Google Scholar]
  30. Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon: fast and bias-aware quantification of transcript expression using dual-phase inference. Nat Methods 2017; 14:417
     [Google Scholar]
  31. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014; 15:550 [View Article] [PubMed]
     [Google Scholar]
  32. Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 2008; 36:3420–3435 [View Article] [PubMed]
     [Google Scholar]
  33. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002; 3:1–12 [View Article] [PubMed]
     [Google Scholar]
  34. Catto MA, Mugerwa H, Myers BK, Pandey S, Dutta B et al. A review on transcriptional responses of interactions between insect vectors and plant viruses. Cells 2022; 11:693 [View Article] [PubMed]
     [Google Scholar]
  35. Lee JH, Choi JY, Tao XY, Kim JS, Kim W et al. Transcriptome analysis of the small brown planthopper, Laodelphax striatellus carrying rice stripe virus. Plant Pathol J 2013; 29:330–337 [View Article] [PubMed]
     [Google Scholar]
  36. Zhai Y, Zhang J, Sun Z, Dong X, He Y et al. Proteomic and transcriptomic analyses of fecundity in the brown planthopper Nilaparvata lugens (Stål). J Proteome Res 2013; 12:5199–5212 [View Article] [PubMed]
     [Google Scholar]
  37. Roy S, Saha TT, Zou Z, Raikhel AS. Regulatory pathways controlling female insect reproduction. Annu Rev Entomol 2018; 63:489–511 [View Article] [PubMed]
     [Google Scholar]
  38. Ding TB, Li J, Chen EH, Niu JZ, Chu D. Transcriptome profiling of the whitefly Bemisia tabaci MED in response to single infection of Tomato yellow leaf curl virus, Tomato chlorosis virus, and their co-infection. Front Physiol 2019; 10:302 [View Article] [PubMed]
     [Google Scholar]
  39. Guo J-Y, Dong S-Z, Yang X, Cheng L, Wan F-H et al. Enhanced vitellogenesis in a whitefly via feeding on a begomovirus-infected plant. PLoS One 2012; 7:e43567 [View Article] [PubMed]
     [Google Scholar]
  40. Su Q, Preisser EL, Zhou XM, Xie W, Liu BM et al. Manipulation of host quality and defense by a plant virus improves performance of whitefly vectors. J Econ Entomol 2015; 108:11–19 [View Article] [PubMed]
     [Google Scholar]
  41. Ziegler-Graff V. Molecular insights into host and vector manipulation by plant viruses. Viruses 2020; 12:263 [View Article] [PubMed]
     [Google Scholar]
  42. Lehman W, Galińska-Rakoczy A, Hatch V, Tobacman LS, Craig R. Structural basis for the activation of muscle contraction by troponin and tropomyosin. J Mol Biol 2009; 388:673–681 [View Article] [PubMed]
     [Google Scholar]
  43. Guerra PA. Evaluating the life-history trade-off between dispersal capability and reproduction in wing dimorphic insects: a meta-analysis. Biol Rev Camb Philos Soc 2011; 86:813–835 [View Article] [PubMed]
     [Google Scholar]
  44. Denno RF, Olmstead KL, McCloud ES. Reproductive cost of flight capability: a comparison of life history traits in wing dimorphic planthoppers. Ecol Entomol 1989; 14:31–44 [View Article]
     [Google Scholar]
  45. Ge S, Sun X, He W, Wyckhuys KAG, He L et al. Potential trade-offs between reproduction and migratory flight in Spodoptera frugiperda. J Insect Physiol 2021; 132:104248 [View Article] [PubMed]
     [Google Scholar]
  46. Zhang Y, Wu K, Wyckhuys KAG, Heimpel GE. Trade-offs between flight and fecundity in the soybean aphid (Hemiptera: Aphididae). J Econ Entomol 2009; 102:133–138 [View Article] [PubMed]
     [Google Scholar]
  47. Samietz J, Köhler G. A fecundity cost of (walking) mobility in an insect. Ecol Evol 2012; 2:2788–2793 [View Article] [PubMed]
     [Google Scholar]
  48. Rygg TD. Flight of Oscinella Frit L. (Diptera, Chloropidae) females in relation to age and ovary development. Entomologia Exp Applicata 1966; 9:74–84 [View Article]
     [Google Scholar]
  49. Hughes CL, Hill JK, Dytham C. Evolutionary trade-offs between reproduction and dispersal in populations at expanding range boundaries. Proc R Soc Lond B 2003; 270:S147–S150 [View Article]
     [Google Scholar]
  50. Stafford CA, Walker GP, Creamer R. Stylet penetration behavior resulting in inoculation of beet severe curly top virus by beet leafhopper, Circulifertenellus. Entomologia Exp Applicata 2009; 130:130–137 [View Article]
     [Google Scholar]
  51. Agianian B, Krzic U, Qiu F, Linke WA, Leonard K et al. A troponin switch that regulates muscle contraction by stretch instead of calcium. EMBO J 2004; 23:772–779 [View Article] [PubMed]
     [Google Scholar]
  52. Cammarato A, Hatch V, Saide J, Craig R, Sparrow JC et al. Drosophila muscle regulation characterized by electron microscopy and three-dimensional reconstruction of thin filament mutants. Biophys J 2004; 86:1618–1624 [View Article] [PubMed]
     [Google Scholar]
  53. Rihani K, Ferveur J-F, Briand L. The 40-year mystery of insect odorant-binding proteins. Biomolecules 2021; 11:509 [View Article] [PubMed]
     [Google Scholar]
  54. Beckage NE. eds Insect Immunology Academic Press; 2008
     [Google Scholar]
  55. Rosales C, Vonnie S. Cellular and molecular mechanisms of insect immunity. Insect physiology and ecology 2017; 10:182–190
     [Google Scholar]
  56. Wang M, Hu Z. Cross-talking between baculoviruses and host insects towards a successful infection. Phil Trans R Soc B 2019; 374:20180324 [View Article]
     [Google Scholar]
  57. Kingsolver MB, Huang Z, Hardy RW. Insect antiviral innate immunity: pathways, effectors, and connections. J Mol Biol 2013; 425:4921–4936 [View Article] [PubMed]
     [Google Scholar]
  58. Marques JT, Imler JL. The diversity of insect antiviral immunity: insights from viruses. Curr Opin Microbiol 2016; 32:71–76 [View Article] [PubMed]
     [Google Scholar]
  59. Wang Q, Yin M, Yuan C, Liu X, Hu Z et al. Identification of a Conserved Prophenoloxidase Activation Pathway in Cotton Bollworm Helicoverpa armigera. Front Immunol 2020; 11:785 [View Article] [PubMed]
     [Google Scholar]
  60. Yuan C, Xing L, Wang M, Wang X, Yin M et al. Inhibition of melanization by serpin-5 and serpin-9 promotes baculovirus infection in cotton bollworm Helicoverpa armigera. PLoS Pathog 2017; 13:e1006645 [View Article] [PubMed]
     [Google Scholar]
  61. Luan J-B, Li J-M, Varela N, Wang Y-L, Li F-F et al. Global analysis of the transcriptional response of whitefly to tomato yellow leaf curl China virus reveals the relationship of coevolved adaptations. J Virol 2011; 85:3330–3340 [View Article] [PubMed]
     [Google Scholar]
  62. Bourne Y, Henrissat B. Glycoside hydrolases and glycosyltransferases: families and functional modules. Curr Opin Struct Biol 2001; 11:593–600 [View Article] [PubMed]
     [Google Scholar]
  63. Xu J, Huang X. Lipid metabolism at membrane contacts: dynamics and functions beyond lipid homeostasis. Front Cell Dev Biol 2020; 8:615856 [View Article] [PubMed]
     [Google Scholar]
  64. Xu Y, Zhou W, Zhou Y, Wu J, Zhou X. Transcriptome and comparative gene expression analysis of Sogatella furcifera (Horváth) in response to southern rice black-streaked dwarf virus. PLoS One 2012; 7:e36238 [View Article]
     [Google Scholar]
  65. Zhang Z, Zhang P, Li W, Zhang J, Huang F et al. De novo transcriptome sequencing in Frankliniella occidentalis to identify genes involved in plant virus transmission and insecticide resistance. Genomics 2013; 101:296–305 [View Article] [PubMed]
     [Google Scholar]
  66. Li M, Zhao J, Su Y-L. Transcriptome analysis of gene expression profiles of tomato yellow leaf curl virus-infected whiteflies over different viral acquisition access periods. Insects 2020; 11:297 [View Article] [PubMed]
     [Google Scholar]
  67. Rubinstein G, Czosnek H. 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 1997; 78:2683–2689 [View Article] [PubMed]
     [Google Scholar]
  68. Czosnek H, Hariton-Shalev A, Sobol I, Gorovits R, Ghanim M. The incredible journey of begomoviruses in their whitefly vector. Viruses 2017; 9:273 [View Article] [PubMed]
     [Google Scholar]
  69. Huang N, Wu W, Yang K, Passarelli AL, Rohrmann GF et al. Baculovirus infection induces a DNA damage response that is required for efficient viral replication. J Virol 2011; 85:12547–12556 [View Article] [PubMed]
     [Google Scholar]
  70. Lomberk G, Wallrath L, Urrutia R. The heterochromatin protein 1 family. Genome Biol 2006; 7:228 [View Article] [PubMed]
     [Google Scholar]
  71. Pandey N, Black BE. Rapid detection and signaling of DNA damage by PARP-1. Trends Biochem Sci 2021; 46:744–757 [View Article] [PubMed]
     [Google Scholar]
  72. Everett H, McFadden G. Apoptosis: an innate immune response to virus infection. Trends Microbiol 1999; 7:160–165 [View Article] [PubMed]
     [Google Scholar]
  73. Wang H, Gort T, Boyle DL, Clem RJ. Effects of manipulating apoptosis on Sindbis virus infection of Aedes aegypti mosquitoes. J Virol 2012; 86:6546–6554 [View Article] [PubMed]
     [Google Scholar]
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Beet curly top virus affects vector biology: the first transcriptome analysis of the beet leafhopper
J. Gen. Virol. 105, 002012 (2024); https://doi.org/10.1099/jgv.0.002012
/content/journal/jgv/10.1099/jgv.0.002012
/content/journal/jgv/10.1099/jgv.0.002012
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