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Volume 104, Issue 4

Engineering aphid transmission of foxtail mosaic virus in the presence of potyvirus helper component proteinase through coat protein modifications No Access

Abstract

Biotechnologies that use plant viruses as plant enhancement tools have shown great potential to flexibly engineer crop traits, but field applications of these technologies are still limited by efficient dissemination methods. Potyviruses can be rapidly inoculated into plants by aphid vectors due to the presence of the potyviral helper component proteinase (HC-Pro), which binds to the DAG motif of the coat protein (CP) of the virion. Previously it was determined that a naturally occurring DAG motif in the non-aphid-transmissible potexvirus, potato aucuba mosaic virus (PAMV), is functional when a potyviral HC-Pro is provided to aphids in plants. The DAG motif of PAMV was successfully transferred to the CP of another non-aphid-transmissible potexvirus, potato virus X, to convey aphid transmission capabilities in the presence of HC-Pro. Here, we demonstrate that DAG-containing segments of the CP from two different potyviruses (sugarcane mosaic virus and turnip mosaic virus), and from the previously used potexvirus, PAMV, can make the potexvirus, foxtail mosaic virus (FoMV), aphid-transmissible when fused with the FoMV CP. We show that DAG-containing FoMVs are transmissible by aphids that have prior access to HC-Pro through potyvirus-infected plants or ectopic expression of HC-Pro. The transmission efficiency of the DAG-containing FoMVs varied from less than 10 % to over 70 % depending on the length and composition of the surrounding amino acid sequences of the DAG-containing segment, as well as due to the recipient plant species. Finally, we show that the engineered aphid-transmissible FoMV is still functional as a plant enhancement resource, as endogenous host target genes were silenced in FoMV-infected plants after aphid transmission. These results suggest that aphid transmission could be engineered into non-aphid-transmissible plant enhancement viral resources to facilitate their field applications.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): aphids , coat protein , DAG motif , genetic engineering , HC-Pro , potexvirus , potyvirus and virus transmission
Funding
This study was supported by the:
  • National Institute of Food and Agriculture (Award 2020-67034-31787)
    • Principle Award Recipient: T. NihranzChad
  • Division of Integrative Organismal Systems (Award 1723926)
    • Principle Award Recipient: ClareL Casteel
  • Defense Sciences Office, DARPA (Award HR0011-17-2-0053)
    • Principle Award Recipient: ClareL Casteel
© 2023 The Authors
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2023-04-13
2024-05-14
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References

  1. Lacomme C. Strategies for altering plant traits using virus-induced gene silencing technologies. Mysore KS, Senthil-Kumar M. Plant Gene Silencing: Methods and Protocols New York, NY: Springer New York; 201525–41
     [Google Scholar]
  2. Zaidi SS-E-A, Mansoor S. Viral vectors for plant genome engineering. Front Plant Sci 2017; 8:539 [View Article] [PubMed]
     [Google Scholar]
  3. Wang M, Gao S, Zeng W, Yang Y, Ma J et al. Plant virology delivers diverse toolsets for biotechnology. Viruses 2020; 12:1338 [View Article] [PubMed]
     [Google Scholar]
  4. Gadhave KR, Gautam S, Rasmussen DA, Srinivasan R. Aphid transmission of Potyvirus: the largest plant-infecting RNA virus genus. Viruses 2020; 12:773 [View Article] [PubMed]
     [Google Scholar]
  5. Ray S, Casteel CL. Effector-mediated plant-virus-vector interactions. Plant Cell 2022; 34:1514–1531 [View Article] [PubMed]
     [Google Scholar]
  6. Bak A, Cheung AL, Yang C, Whitham SA, Casteel CL. A viral protease relocalizes in the presence of the vector to promote vector performance. Nat Commun 2017; 8:14493 [View Article] [PubMed]
     [Google Scholar]
  7. Casteel CL, Yang C, Nanduri AC, De Jong HN, Whitham SA et al. The NIa-Pro protein of Turnip mosaic virus improves growth and reproduction of the aphid vector, Myzus persicae (green peach aphid). Plant J 2014; 77:653–663 [View Article] [PubMed]
     [Google Scholar]
  8. Casteel CL, De Alwis M, Bak A, Dong H, Whitham SA et al. Disruption of ethylene responses by Turnip mosaic virus mediates suppression of plant defense against the green peach aphid vector. Plant Physiol 2015; 169:209–218 [View Article] [PubMed]
     [Google Scholar]
  9. Zhao Y, Cao X, Zhong W, Zhou S, Li Z et al. A viral protein orchestrates rice ethylene signaling to coordinate viral infection and insect vector-mediated transmission. Mol Plant 2022; 15:689–705 [View Article] [PubMed]
     [Google Scholar]
  10. Tungadi T, Groen SC, Murphy AM, Pate AE, Iqbal J et al. Cucumber mosaic virus and its 2b protein alter emission of host volatile organic compounds but not aphid vector settling in tobacco. Virol J 2017; 14:91 [View Article] [PubMed]
     [Google Scholar]
  11. Guo H, Gu L, Liu F, Chen F, Ge F et al. Aphid-borne viral spread is enhanced by virus-induced accumulation of plant reactive oxygen species. Plant Physiol 2019; 179:143–155 [View Article] [PubMed]
     [Google Scholar]
  12. 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]
  13. Jayasinghe WH, Kim H, Nakada Y, Masuta C. A plant virus satellite RNA directly accelerates wing formation in its insect vector for spread. Nat Commun 2021; 12:7087 [View Article] [PubMed]
     [Google Scholar]
  14. Chay CA, Gunasinge UB, Dinesh-Kumar SP, Miller WA, Gray SM. Aphid transmission and systemic plant infection determinants of barley yellow dwarf luteovirus-PAV are contained in the coat protein readthrough domain and 17-kDa protein, respectively. Virology 1996; 219:57–65 [View Article] [PubMed]
     [Google Scholar]
  15. Wang JY, Chay C, Gildow FE, Gray SM. Readthrough protein associated with virions of barley yellow dwarf luteovirus and its potential role in regulating the efficiency of aphid transmission. Virology 1995; 206:954–962 [View Article] [PubMed]
     [Google Scholar]
  16. Blanc S, Drucker M, Uzest M. Localizing viruses in their insect vectors. Annu Rev Phytopathol 2014; 52:403–425 [View Article] [PubMed]
     [Google Scholar]
  17. Hoh F, Uzest M, Drucker M, Plisson-Chastang C, Bron P et al. Structural insights into the molecular mechanisms of cauliflower mosaic virus transmission by its insect vector. J Virol 2010; 84:4706–4713 [View Article] [PubMed]
     [Google Scholar]
  18. Plisson C, Uzest M, Drucker M, Froissart R, Dumas C et al. Structure of the mature P3-virus particle complex of cauliflower mosaic virus revealed by cryo-electron microscopy. J Mol Biol 2005; 346:267–277 [View Article] [PubMed]
     [Google Scholar]
  19. Blanc S, Ammar ED, Garcia-Lampasona S, Dolja VV, Llave C et al. Mutations in the potyvirus helper component protein: effects on interactions with virions and aphid stylets. J Gen Virol 1998; 79 (Pt 12):3119–3122 [View Article] [PubMed]
     [Google Scholar]
  20. Peng YH, Kadoury D, Gal-On A, Huet H, Wang Y et al. Mutations in the HC-Pro gene of zucchini yellow mosaic potyvirus: effects on aphid transmission and binding to purified virions. J Gen Virol 1998; 79 (Pt 4):897–904 [View Article] [PubMed]
     [Google Scholar]
  21. López-Moya JJ, Wang RY, Pirone TP. Context of the coat protein DAG motif affects potyvirus transmissibility by aphids. J Gen Virol 1999; 80 (Pt 12):3281–3288 [View Article] [PubMed]
     [Google Scholar]
  22. Nigam D, LaTourrette K, Souza PFN, Garcia-Ruiz H. Genome-wide variation in potyviruses. Front Plant Sci 2019; 10:1439 [View Article] [PubMed]
     [Google Scholar]
  23. Bouton C, King RC, Chen H, Azhakanandam K, Bieri S et al. Foxtail mosaic virus: a viral vector for protein expression in cereals. Plant Physiol 2018; 177:1352–1367 [View Article] [PubMed]
     [Google Scholar]
  24. Liu N, Xie K, Jia Q, Zhao J, Chen T et al. Foxtail mosaic virus-induced gene silencing in monocot plants. Plant Physiol 2016; 171:1801–1807 [View Article] [PubMed]
     [Google Scholar]
  25. Mei Y, Zhang C, Kernodle BM, Hill JH, Whitham SA. A Foxtail mosaic virus vector for virus-induced gene silencing in maize. Plant Physiol 2016; 171:760–772 [View Article] [PubMed]
     [Google Scholar]
  26. Mei Y, Beernink BM, Ellison EE, Konečná E, Neelakandan AK et al. Protein expression and gene editing in monocots using foxtail mosaic virus vectors. Plant Direct 2019; 3:e00181 [View Article] [PubMed]
     [Google Scholar]
  27. Baulcombe DC, Lloyd J, Manoussopoulos IN, Roberts IM, Harrison BD. Signal for potyvirus-dependent aphid transmission of potato aucuba mosaic virus and the effect of its transfer to potato virus X. J Gen Virol 1993; 74 (Pt 7):1245–1253 [View Article] [PubMed]
     [Google Scholar]
  28. Kassanis B. The transmission of potato aucuba mosaic virus by aphids from plants also infected by potato viruses A or Y. Virology 1961; 13:93–97 [View Article] [PubMed]
     [Google Scholar]
  29. Kassanis B, Govier DA. New evidence on the mechanism of aphid transmission of potato C and potato aucuba mosaic viruses. J Gen Virol 1971; 10:99–101 [View Article] [PubMed]
     [Google Scholar]
  30. Cabanillas DG, Jiang J, Movahed N, Germain H, Yamaji Y et al. Turnip mosaic virus uses the SNARE protein VTI11 in an unconventional route for replication vesicle trafficking. Plant Cell 2018; 30:2594–2615 [View Article] [PubMed]
     [Google Scholar]
  31. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402–408 [View Article] [PubMed]
     [Google Scholar]
  32. Sokal R, Rohlf F. Biometry: the principles and practice of statistics in biological research. SERBIULA (sistema Librum 20) 2013
     [Google Scholar]
  33. Atreya PL, Atreya CD, Pirone TP. Amino acid substitutions in the coat protein result in loss of insect transmissibility of a plant virus. Proc Natl Acad Sci U S A 1991; 88:7887–7891 [View Article] [PubMed]
     [Google Scholar]
  34. Atreya PL, Lopez-Moya JJ, Chu M, Atreya CD, Pirone TP. Mutational analysis of the coat protein N-terminal amino acids involved in potyvirus transmission by aphids. J Gen Virol 1995; 76 (Pt 2):265–270 [View Article] [PubMed]
     [Google Scholar]
  35. Flasinski S, Cassidy BG. Potyvirus aphid transmission requires helper component and homologous coat protein for maximal efficiency. Arch Virol 1998; 143:2159–2172 [View Article] [PubMed]
     [Google Scholar]
  36. Seo J-K, Kang S-H, Seo BY, Jung JK, Kim K-H. Mutational analysis of interaction between coat protein and helper component-proteinase of Soybean mosaic virus involved in aphid transmission. Mol Plant Pathol 2010; 11:265–276 [View Article] [PubMed]
     [Google Scholar]
  37. He Z, Wu J, Sun X, Dai M. The Maize clade A PP2C phosphatases play critical roles in multiple abiotic stress responses. Int J Mol Sci 2019; 20:3573 [View Article] [PubMed]
     [Google Scholar]
  38. López-Moya JJ, Wang RY, Pirone TP. Context of the coat protein DAG motif affects potyvirus transmissibility by aphids. J Gen Virol 1999; 80 (Pt 12):3281–3288 [View Article] [PubMed]
     [Google Scholar]
  39. Bokx JA, Hoof HA, Piron PGM. Relation between concentration of potato virus YN and its availability to Myzus persicae. Netherlands J Plant Pathol 1978; 84:95–100 [View Article]
     [Google Scholar]
  40. Arazi T, Shiboleth YM, Gal-On A. A nonviral peptide can replace the entire N terminus of zucchini yellow mosaic potyvirus coat protein and permits viral systemic infection. J Virol 2001; 75:6329–6336 [View Article] [PubMed]
     [Google Scholar]
  41. López-Moya JJ, Pirone TP. Charge changes near the N terminus of the coat protein of two potyviruses affect virus movement. J Gen Virol 1998; 79:161–165 [View Article] [PubMed]
     [Google Scholar]
  42. Sako N, Ogata K. Different helper factors associated with aphid transmission of some potyviruses. Virology 1981; 112:762–765 [View Article] [PubMed]
     [Google Scholar]
  43. Dombrovsky A, Huet H, Chejanovsky N, Raccah B. Aphid transmission of a potyvirus depends on suitability of the helper component and the N terminus of the coat protein. Arch Virol 2005; 150:287–298 [View Article] [PubMed]
     [Google Scholar]
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Engineering aphid transmission of foxtail mosaic virus in the presence of potyvirus helper component proteinase through coat protein modifications
J. Gen. Virol. 104, 001844 (2023); https://doi.org/10.1099/jgv.0.001844
/content/journal/jgv/10.1099/jgv.0.001844
/content/journal/jgv/10.1099/jgv.0.001844
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