Dynamic interactions between plant viruses and their hosts for symptom development

  • Larissa J. OsterbaanEmail author
  • Marc Fuchs


As obligate intracellular parasites, plant viruses catalyze drastic alterations in the cellular physiology of host cells in order to support their own replication. This disruption often, but not always, manifests macroscopically as disease symptoms. The search for what distinguishes symptom-inducing virus strains from their asymptomatic counterparts has long been a central component of plant virology research. A consistent through line has been the conclusion that symptoms arise from specific interactions between viral and host components. The identification of viral components responsible for symptom development (i.e. viral symptom determinants) followed by the identification and characterization of interactions with host components has led to concrete mechanistic linkages between the viral and host interactants for some symptoms. The rise of systems biology approaches (e.g. transcriptomics and proteomics) has allowed host responses to be described in greater detail, providing a broad view of the molecular events of plant virus infections. Here, we review the most recent literature describing plant virus symptom determinants. This includes studies detailing specific virus-host interactions which lead to symptom development, as well as those which utilize systems biology approaches such as transcriptomics to probe the molecular changes underlying the development of virus symptoms. Emerging trends, and how they might inform the future of plant virus symptomatology research, are discussed.


Plant virus Symptoms Symptom determinant Transcriptomics Chimeras Temperature Environment Reverse genetics Virus-host interactions 



Thanks are due to E.J. Cieniewicz for her helpful and encouraging discussions during the preparation of this review and to the library services staff of the Albert. R. Mann Library of Cornell University for their guidance in literature database search strategies.


This work was funded by a Schmittau-Novak Integrative Plant Science grant from the Cornell University School of Integrative Plant Science, the AFRI NIFA Fellowships Grant Program [grant no. 2018–67011-28107/project accession no. 1015454] from the USDA National Institute of Food and Agriculture, Federal Capacity Funds, and Cornell AgriTech’s Research Venture Funds.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Basu S, Kumar Kushwaha N, Kumar Singh A et al (2018) Dynamics of a geminivirus-encoded pre-coat protein and host RNA-dependent RNA polymerase 1 in regulating symptom recovery in tobacco. J Exp Bot 69:2085–2102. CrossRefGoogle Scholar
  2. Betts MJ, Russell RB (2007) Amino-acid properties and consequences of substitutions. In: Barnes MR (ed) Bioinformatics for geneticists. John Wiley & Sons, Ltd, Chichester, pp 311–342CrossRefGoogle Scholar
  3. Chen X-R, Wang Y, Zhao H-H et al (2018) Brassica yellows virus’ movement protein upregulates anthocyanin accumulation, leading to the development of purple leaf symptoms on Arabidopsis thaliana. Sci Rep 8:16273. CrossRefGoogle Scholar
  4. Chung BN, Canto T, Tenllado F et al (2016) The effects of high temperature on infection by Potato virus Y, Potato virus A, and Potato leafroll virus. Plant Pathol J 32:321–328. CrossRefGoogle Scholar
  5. Chung BN, Lee J-H, Kang B-C et al (2018) HR-mediated defense response is overcome at high temperatures in Capsicum species. Plant Pathol J 34:71–77. Google Scholar
  6. Culver JN, Padmanabhan MS (2007) Virus-induced disease: altering host physiology one interaction at a time. Annu Rev Phytopathol 45:221–243. CrossRefGoogle Scholar
  7. del Toro FJ, Rakhshandehroo F, Larruy B et al (2017) Effects of simultaneously elevated temperature and CO2 levels on Nicotiana benthamiana and its infection by different positive-sense RNA viruses are cumulative and virus type-specific. Virology 511:184–192. CrossRefGoogle Scholar
  8. Fujita N, Komatsu K, Ayukawa Y et al (2018) N-terminal region of cysteine-rich protein (CRP) in carlaviruses is involved in the determination of symptom types. Mol Plant Pathol 19:180–190. CrossRefGoogle Scholar
  9. García JA, Pallás V (2015) Viral factors involved in plant pathogenesis. Curr Opin Virol 11:21–30. CrossRefGoogle Scholar
  10. Gellért Á, Pósa T, Fábián A et al (2018) A single point mutation on the cucumber mosaic virus surface induces an unexpected and strong interaction with the F1 complex of the ATP synthase in Nicotiana clevelandii plants. Virus Res 251:47–55. CrossRefGoogle Scholar
  11. Godfrey S, Settumba M, Samuel K (2017) Effect of temperature on sweet potato virus disease symptom expression. Afr J Agric Res 12:2295–2309. CrossRefGoogle Scholar
  12. Gomez MA, Lin ZD, Moll T et al (2019) Simultaneous CRISPR/Cas9-mediated editing of cassava eIF4E isoforms nCBP-1 and nCBP-2 reduces cassava brown streak disease symptom severity and incidence. Plant Biotechnol J 17:421–434. CrossRefGoogle Scholar
  13. Gómez-Aix C, Pascual L, Cañizares J et al (2016) Transcriptomic profiling of Melon necrotic spot virus-infected melon plants revealed virus strain and plant cultivar-specific alterations. BMC Genomics 17:429. CrossRefGoogle Scholar
  14. Han S-H, Park J-S, Han J-Y et al (2017) New Korean isolates of Pepper mild mottle virus (PMMoV) differ in symptom severity and subcellular localization of the 126 kDa protein. Virus Genes 53:434–445. CrossRefGoogle Scholar
  15. Hashimoto M, Komatsu K, Iwai R et al (2015) Cell death triggered by a putative amphipathic helix of Radish mosaic virus helicase protein is tightly correlated with host membrane modification. Mol Plant-Microbe Interact 28:675–688. CrossRefGoogle Scholar
  16. Hasiów-Jaroszewska B, Borodynko N, Jackowiak P et al (2011) Single mutation converts mild pathotype of the Pepino mosaic virus into necrotic one. Virus Res 159:57–61. CrossRefGoogle Scholar
  17. Hirata H, Lu X, Yamaji Y et al (2003) A single silent substitution in the genome of apple stem grooving virus causes symptom attenuation. J Gen Virol 84:2579–2583CrossRefGoogle Scholar
  18. Kassanis B (1952) Some effects of high temperature on the susceptibility of plants to infection with viruses. Ann Appl Biol 39:358–369. CrossRefGoogle Scholar
  19. Krause-Sakate R, Redondo E, Richard-Forget F et al (2005) Molecular mapping of the viral determinants of systemic wilting induced by a Lettuce mosaic virus (LMV) isolate in some lettuce cultivars. Virus Res 109:175–180. CrossRefGoogle Scholar
  20. Lan Y, Li Y, E Z et al (2018) Identification of virus-derived siRNAs and their targets in RBSDV-infected rice by deep sequencing. J Basic Microbiol 58:227–237. CrossRefGoogle Scholar
  21. Li H, Zeng R, Chen Z et al (2018) S-acylation of a geminivirus C4 protein is essential for regulating the CLAVATA pathway in symptom determination. J Exp Bot 69:4459–4468. CrossRefGoogle Scholar
  22. Lim H-S, Nam J, Seo E-Y et al (2014) The coat protein of Alternanthera mosaic virus is the elicitor of a temperature-sensitive systemic necrosis in Nicotiana benthamiana, and interacts with a host boron transporter protein. Virology 452–453:264–278. CrossRefGoogle Scholar
  23. Liu L, Peng B, Zhang Z et al (2017) Exploring different mutations at a single amino acid position of Cucumber green mottle mosaic virus replicase to attain stable symptom attenuation. Phytopathology 107:1080–1086. CrossRefGoogle Scholar
  24. Madroñero J, Rodrigues SP, Antunes TFS et al (2018) Transcriptome analysis provides insights into the delayed sticky disease symptoms in Carica papaya. Plant Cell Rep 37:967–980. CrossRefGoogle Scholar
  25. Margaria P, Anderson CT, Turina M, Rosa C (2016) Identification of Ourmiavirus 30K movement protein amino acid residues involved in symptomatology, viral movement, subcellular localization and tubule formation. Mol Plant Pathol 17:1063–1079. CrossRefGoogle Scholar
  26. Martin IR, Vigne E, Berthold F et al (2018) The 50 distal amino acids of the 2AHP homing protein of Grapevine fanleaf virus elicit a hypersensitive reaction on Nicotiana occidentalis. Mol Plant Pathol 19:731–743. CrossRefGoogle Scholar
  27. Masinde EA, Mkamillo G, Ogendo JO et al (2018) Genotype by environment interactions in identifying cassava (Manihot esculenta Crantz) resistant to cassava brown streak disease. Field Crop Res 215:39–48. CrossRefGoogle Scholar
  28. Minicka J, Rymelska N, Elena SF et al (2015) Molecular evolution of Pepino mosaic virus during long-term passaging in different hosts and its impact on virus virulence. Ann Appl Biol 166:389–401. CrossRefGoogle Scholar
  29. Obrepalska-Steplowska A, Zmienko A, Wrzesinska B et al (2018) The defense response of Nicotiana benthamiana to peanut stunt virus infection in the presence of symptom exacerbating satellite RNA. Viruses 10:449. CrossRefGoogle Scholar
  30. Osterbaan LJ, Choi J, Kenney J et al (2019) The identity of a single residue of the RNA-dependent RNA polymerase of grapevine fanleaf virus modulates vein clearing symptoms in Nicotiana benthamiana. Mol Plant-Microbe Interact.
  31. Pallas V, García JA (2011) How do plant viruses induce disease? Interactions and interference with host components. J Gen Virol 92:2691–2705CrossRefGoogle Scholar
  32. Paudel DB, Sanfaçon H (2018) Exploring the diversity of mechanisms associated with plant tolerance to virus infection. Front Plant Sci 9:1575. CrossRefGoogle Scholar
  33. Qiu Y, Zhang Y, Hu F, Zhu S (2017) Characterization of siRNAs derived from cucumber mosaic virus in infected tobacco plants. Arch Virol 162:2077–2082. CrossRefGoogle Scholar
  34. Qiu Y, Zhang Y, Wang C et al (2018) Cucumber mosaic virus coat protein induces the development of chlorotic symptoms through interacting with the chloroplast ferredoxin I protein. Sci Rep 8:1205. CrossRefGoogle Scholar
  35. Ramesh SV, Williams S, Kappagantu M et al (2017) Transcriptome-wide identification of host genes targeted by tomato spotted wilt virus-derived small interfering RNAs. Virus Res 238:13–23. CrossRefGoogle Scholar
  36. Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45. CrossRefGoogle Scholar
  37. Rodríguez-Cerezo E, Klein PG, Shaw JG (1991) A determinant of disease symptom severity is located in the 3′-terminal noncoding region of the RNA of a plant virus. Proc Natl Acad Sci 88:9863–9867. CrossRefGoogle Scholar
  38. Rong W, Wang X, Wang X et al (2018) Molecular and ultrastructural mechanisms underlying yellow dwarf symptom formation in wheat after infection of barley yellow dwarf virus. Int J Mol Sci 19:1187. CrossRefGoogle Scholar
  39. Salánki K, Kiss L, Gellért Á, Balázs E (2011) Identification a coat protein region of cucumber mosaic virus (CMV) essential for long-distance movement in cucumber. Arch Virol 156:2279–2283. CrossRefGoogle Scholar
  40. Sánchez F, Manrique P, Mansilla C et al (2015) Viral strain-specific differential alterations in Arabidopsis developmental patterns. Mol Plant-Microbe Interact 28:1304–1315. CrossRefGoogle Scholar
  41. Selman I, Grant SA (1957) The influence of temperature and daylength on spotted wilt virus disease of tomato. Ann Appl Biol 45:312–317. CrossRefGoogle Scholar
  42. Seo J-K, Kwak H-R, Choi B et al (2017) Movement protein of broad bean wilt virus 2 serves as a determinant of symptom severity in pepper. Virus Res 242:141–145. CrossRefGoogle Scholar
  43. Shi B, Lin L, Wang S et al (2016) Identification and regulation of host genes related to Rice stripe virus symptom production. New Phytol 209:1106–1119. CrossRefGoogle Scholar
  44. Shimura H, Pantaleo V, Ishihara T et al (2011) A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery. PLoS Pathog 7:1–12. CrossRefGoogle Scholar
  45. Smith NA, Eamens AL, Wang M-B (2011) Viral small interfering RNAs target host genes to mediate disease symptoms in plants. PLoS Pathog 7.
  46. Tatineni S, Elowsky C, Graybosch RA (2017) Wheat streak mosaic virus coat protein deletion mutants elicit more severe symptoms than wild-type virus in multiple cereal hosts. Mol Plant-Microbe Interact 30:974–983. CrossRefGoogle Scholar
  47. Tatineni S, McMechan AJ, Hein GL (2018) Wheat streak mosaic virus coat protein is a determinant for vector transmission by the wheat curl mite. Virology 514:42–49. CrossRefGoogle Scholar
  48. Vigne E, Gottula JW, Schmitt-Keichinger C et al (2013) A strain-specific segment of the RNA-dependent RNA polymerase of grapevine fanleaf virus determines symptoms in Nicotiana species. J Gen Virol 94:2803–2813. CrossRefGoogle Scholar
  49. Wang S, Cui W, Wu X et al (2018) Suppression of nbe-miR166h-p5 attenuates leaf yellowing symptoms of potato virus X on Nicotiana benthamiana and reduces virus accumulation. Mol Plant Pathol 19:2384–2396. CrossRefGoogle Scholar
  50. Wieczorek P, Obrępalska-Stęplowska A (2016) The N-terminal fragment of the tomato torrado virus RNA1-encoded polyprotein induces a hypersensitive response (HR)-like reaction in Nicotiana benthamiana. Arch Virol 161:1849–1858. CrossRefGoogle Scholar
  51. Wosula EN, Tatineni S, Wegulo SN, Hein GL (2016) Effect of temperature on wheat streak mosaic disease development in winter wheat. Plant Dis 101:324–330. CrossRefGoogle Scholar
  52. Xu Y, Da Silva WL, Qian Y, Gray SM (2018) An aromatic amino acid and associated helix in the C-terminus of the potato leafroll virus minor capsid protein regulate systemic infection and symptom expression. PLoS Pathog 14:1–30. Google Scholar
  53. Yang C, Guo R, Jie F et al (2007) Spatial analysis of Arabidopsis thaliana gene expression in response to Turnip mosaic virus infection. Mol Plant-Microbe Interact 20:358–370. CrossRefGoogle Scholar
  54. Yang Y, Liu T, Shen D, et al (2019) Tomato yellow leaf curl virus intergenic siRNAs target a host long noncoding RNA to modulate disease symptoms. PLoS One 1–22.
  55. Zavallo D, Debat HJ, Conti G et al (2015) Differential mRNA accumulation upon early Arabidopsis thaliana infection with ORMV and TMV-Cg is associated with distinct endogenous small RNAs level. PLoS One 10:1–24. CrossRefGoogle Scholar
  56. Zhan B, Zhao W, Li S et al (2018) Functional scanning of apple geminivirus proteins as symptom determinants and suppressors of posttranscriptional gene silencing. Viruses 10:488. CrossRefGoogle Scholar
  57. Zhang H, Sonnewald U (2017) Differences and commonalities of plant responses to single and combined stresses. Plant J 90:839–855. CrossRefGoogle Scholar
  58. Zhang X-P, Liu D-S, Yan T et al (2017) Cucumber mosaic virus coat protein modulates the accumulation of 2b protein and antiviral silencing that causes symptom recovery in planta. PLoS Pathog 13:1–25. Google Scholar
  59. Zhao F, Li Y, Chen L et al (2016) Temperature dependent defence of Nicotiana tabacum against Cucumber mosaic virus and recovery occurs with the formation of dark green islands. J Plant Biol 59:293–301. CrossRefGoogle Scholar
  60. Zhong X, Wang ZQ, Xiao R et al (2017) Mimic phosphorylation of a βC1 protein encoded by TYLCCNB impairs its functions as a viral suppressor of RNA silencing and a symptom determinant. J Virol 91.

Copyright information

© Società Italiana di Patologia Vegetale (S.I.Pa.V.) 2019

Authors and Affiliations

  1. 1.Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell UniversityCornell AgriTech at the New York State Agricultural Experiment StationGenevaUSA

Personalised recommendations