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Serological and molecular analysis indicates the presence of distinct viral genotypes of Apple stem pitting virus in India

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Abstract

Recombination leads to the generation of new viral progeny which remain undetected by routine testing procedures and may be a threat to the infected host. Here, we have characterised the complete genome sequences of two isolates of Apple stem pitting virus from apple cv. Red Chief (Palampur) and cv. Gold Spur (N) with distinct serological reactivities. The viral genomes consisted of 9267 nucleotides for isolate Palampur and 9254 nucleotides for isolate N, excluding the poly (A) tail and contained 5five open reading frames (ORFs). Isolate N shared 80.8% sequence identity with ASPV apple isolate GA2 from China, while isolate Palampur shared 81.4% sequence identity with ASPV apple isolate PB66 from the United Kingdom. The serological difference of isolates N and Palampur along with their low sequence identity indicated the existence of two distinct virus genotypes which was corroborated by evolutionary and genetic differentiation analyses. Recombination events were detected in the RdRp and CP sequences of Palampur isolate thereby suggesting the role of recombination in the evolution of distinct virus genotypes.

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References

  • Adams MJ, Antoniw JF, Bar-Joseph M, Brunt AA, Candresse T, Foster GD, Martelli GP, Milne RG, Zavriev SK, Fauquet CM (2004) The new plant virus family Flexiviridae and assessment of molecular criteria for species demarcation. Arch Virol 149:1045–1060

    Article  CAS  PubMed  Google Scholar 

  • Basso J, Dallaire P, Charest PJ, Devantier Y, Laliberté JF (1994) Evidence for an internal ribosome entry site within the 5’ non-translated region of turnip mosaic potyvirus RNA. J Gen Virol 75:3157–3165

    Article  CAS  PubMed  Google Scholar 

  • Brakta A, Sharma U, Thakur PD, Handa A (2013) First report of pear stony pit disease from India. New Dis Rep 27:11

    Article  Google Scholar 

  • Candresse T, Lanneau M, Revers F, Macquaire G, German S, Dunez J, Grasseau N, Malinovsky T (1995) An immunocapture PCR assay adapted to the detection and the analysis of the molecular variability of Apple chlorotic leaf spot virus. Acta Hortic 386:136–147

    Article  CAS  Google Scholar 

  • Chooi KM, Cohen D, Pearson MN (2013) Molecular characterization of two divergent variants of grapevine leafroll-associated virus 3 in New Zealand. Adv Virol 158:1597–1602

    CAS  Google Scholar 

  • Constable FE, Joyce PA, Rodoni BC (2007) A survey of key Australian pome fruit growing districts for exotic and endemic pathogens. Australas Plant Pathol 36:165–172

    Article  Google Scholar 

  • Dhir S, Tomar M, Thakur PD, Ram R, Hallan V, Zaidi AA (2010) Molecular evidence for Apple stem pitting virus infection in India. Plant Pathol 53:393

    Article  Google Scholar 

  • Dhir S, Ram R, Hallan V, Zaidi AA (2011) Molecular characterization of an Indian variant of Apple stem pitting virus: evidence of recombination. J Plant Pathol 93:471–478

    CAS  Google Scholar 

  • Dhir S, Walia Y, Zaidi AA, Hallan V (2015) A simplified strategy for studying the etiology of viral diseases: Apple stem grooving virus as a case study. J Virol Methods 213:106–110

    Article  CAS  PubMed  Google Scholar 

  • Dhir S, Lakshmi V, Hallan V (2021) Development of immunodiagnostics for Apple stem pitting virus and Apple mosaic virus infecting apple in India. Indian Phytopathol 74:189–199

    Article  Google Scholar 

  • Felsenstein S (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Gadiou S, Kundu JK, Paunovic S, Garcia-Diez P, Komorowska B, Gospodaryk A, Handa A, Massart S, Birisik N, Takur PD, Polischuk V (2010) Genetic diversity of flexiviruses infecting pome fruit trees. J Plant Pathol 92(3):685–691

    CAS  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  CAS  PubMed  Google Scholar 

  • James D, Varga A, Jesperson GD, Navratil M, Safarova D, Constable F, Horner M, Eastwell K, Jelkmann W (2013) Identification and complete genome analysis of a virus variant or putative new foveavirus associated with apple green crinkle disease. Adv Virol 158:1877–1887

    CAS  Google Scholar 

  • Jelkmann W (1994) Nucleotide sequences of Apple stem pitting virus and of the coat protein gene of a similar virus from pear associated with vein yellows disease and their relationship with potex- and carlaviruses. J Gen Virol 75:1535–1545

    Article  CAS  PubMed  Google Scholar 

  • Jelkmann W, Keim-Konrad R (1997) Immuno-capture polymerase chain reaction and plate-trapped ELISA for the detection of Apple stem pitting virus. J Phytopathol 145:499–503

    Article  Google Scholar 

  • Koganezawa H, Yanase H (1990) A new type of elongated virus isolated from apple trees containing the stem pitting agent. Plant Dis 74(8):610–614

    Article  CAS  Google Scholar 

  • Komorowska B, Siedlecki P, Kaczanowski S, Hasiów-Jaroszewska B, Malinowski T (2011) Sequence diversity and potential recombination events in the coat protein gene of Apple stem pitting virus. Virus Res 158:263–267

    Article  CAS  PubMed  Google Scholar 

  • Komorowska B, Hasiów-Jaroszewska B, Elena SF (2019) Evolving by deleting: patterns of molecular evolution of Apple stem pitting virus isolates from Poland. J Gen Virol 100:1442–1456

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Singh RM, Ram R, Badyal J, Hallan V, Zaidi AA, Varma A (2012) Determination of major viral and sub viral pathogens incidence in apple orchards in Himachal Pradesh. Indian J Virol 23:75–79

    Article  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leone G, Linder JL, Van der Meer FA, Schoen CD (1998) Symptoms on apple and pear indicators after back-transmission from Nicotiana occidentalis confirm the identity of Apple stem pitting virus with Pear vein yellows virus. Acta Hort 472:61–65

    Article  Google Scholar 

  • Li Z, Kondo H, Andika IB, Liu P, Sun L, Wu Y (2016) Identification of genome recombination among Apple stem pitting isolates. J Plant Pathol 98:595–601

    Google Scholar 

  • Li C, Yaegashi H, Kishigami R, Kawakubo A, Yamagishi N, Ito T, Yoshikawa N (2020) Apple russet ring and apple green crinkle diseases: fulfillment of Koch’s postulates by virome analysis, amplification of full-length cDNA of viral genomes, in vitro transcription of infectious Viral RNAs, and reproduction of symptoms on fruits of apple trees inoculated with viral RNAs. Front Microbiol 11:1–15

    Google Scholar 

  • Liu N, Niu J, Zhao Y (2012) Complete genomic sequence analyses of Apple stem pitting virus isolates from China. Adv Virol 44:124–130

    CAS  Google Scholar 

  • Liu L, Zheng M-M, Ma X, Li Y, Li Q, Wang G, Hong N (2019) Molecular, serological and biological characterization of a novel Apple stem pitting virus strain from a local pear variety grown in China. J Integr Agric 18(11):2549–2560

    Article  Google Scholar 

  • Ma BG, Niu JX, Morley-Bunker M, Pan LZ, Zhang HP, Zhang LX (2008) Detection of three pear viruses by multiplex RT-PCR assays with co-amplification of an internal control. Australas Plant Pathol 37:117–122

    Article  CAS  Google Scholar 

  • Ma X, Hong N, Moffett P, Wang G (2016) Genetic diversity and evolution of Apple stem pitting virus isolates from pear in China. Can J Plant Pathol 38:218–230

    Article  Google Scholar 

  • Ma X, Hong N, Moffett P, Zhou Y, Wang G (2019) Functional analyses of Apple stem pitting virus coat protein variants. Virol J 16(1):20

    Article  PubMed  PubMed Central  Google Scholar 

  • Magome H, Yoshikawa N, Takahashi T, Ito T, Miyakawa T (1997) Molecular variability of the genomes of capilloviruses from apple, Japanese pear, European pear, and citrus trees. Phytopathology 87:389–396

    Article  CAS  PubMed  Google Scholar 

  • Magome H, Yoshikawa N, Takahashi T (1999) Single-strand conformation polymorphism analysis of Apple stem grooving capillovirus sequence variants. Phytopathology 89:136–140

    Article  CAS  PubMed  Google Scholar 

  • Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1:1–5

    Article  Google Scholar 

  • Mathioudakis MM, Maliogka VI, Dovas CI, Vasilakakis M, Katis NI (2006) First record of the Apple stem pitting virus (ASPV) in quince in Greece. J Plant Pathol 88:221

    Google Scholar 

  • Mathioudakis MM, Maliogka VI, Dovas CI, Paunovic S, Katis NI (2009) Reliable RT-PCR detection of Apple stem pitting virus in pome fruits ant its association with quince fruit deformation disease. Plant Pathol 58:228–236

    Article  CAS  Google Scholar 

  • Mathioudakis MM, Maliogka VI, Katsiani AT, Katis NI (2010) Incidence and molecular variability of Apple stem pitting and Apple chlorotic leaf spot viruses in apple and pear orchards in Greece. J Plant Patho 92:141–149

    Google Scholar 

  • Mathioudakis MM, Candresse T, Barone M, Rogozzino A, Katis NI (2011) Cydonia japonica, Pyrus calleryana and P. amygdaliformis: three new ornamental or wild hosts of Apple stem pitting virus. Virus Genes 44:319–322

    Article  PubMed  Google Scholar 

  • Menzel W, Jelkmann W, Maiss E (2002) Detection of four apple viruses by multiplex RT-PCR assays with co-amplification of plant mRNA as internal control. J Virol Methods 99:81–92

    Article  CAS  PubMed  Google Scholar 

  • Morelli M, Giampetruzzi A, Laghezza L, Catalano L, Savino VN, Saldarelli P (2017) Identification and characterization of an isolate of apple green crinkle associated virus involved in a severe disease of quince (Cydonia oblonga, Mill.). Arch Virol 162:299–306

    Article  CAS  PubMed  Google Scholar 

  • Nagy PD, Bujarski JJ (1996) Homologous RNA recombination in brome mosaic virus: AU-rich sequences decrease the accuracy of crossovers. J Virol 70(1):415–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning A laboratory manual, 2nd edn. Spring Harbor Laboratory, Cold Spring Harbor Laboratory

    Google Scholar 

  • Stouffer RF (1989) Apple stem pitting. In: Fridlund PR (ed) Virus and virus-like diseases of pome fruits and simulating noninfectious disorders. Washington State University Cooperative Extension College, Pullman, pp 138–144

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu ZB, Ku HM, Su CC, Chen IZ, Jan FJ (2010) Molecular and biological characterization of an isolate of Apple stem pitting virus causing pear vein yellows disease in Taiwan. J Plant Pathol 92:721–728

    CAS  Google Scholar 

  • Yang HY, Liu ZJ, Luo S, Li LL (2017) First report of Apple stem pitting virus infecting Nanking cherry in China. Plant Dis 101:1067

    Article  Google Scholar 

  • Yoon JY, Joa JH, San Choi K, Do KS, Lim HC, Chung BN (2014) Genetic diversity of a natural population of Apple stem pitting virus isolated from apple in Korea. Plant Pathol J 30:195–199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshikawa N, Matsuda H, Oda Y, Isogai M, Takahashi T (2001) Genome heterogeneity of Apple stem pitting virus in apple trees. Acta Hortic 550:285–290

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are thankful to the Director, CSIR-Institute of Himalayan Bioresource Technology, Palampur, H.P (India) and Academy of Scientific and Innovative Research, for providing necessary facilities. Financial support from Department of Biotechnology, Govt. of India (BT/PR/11001PBD/16/803/2008) is thankfully acknowledged. This is CSIR-IHBT publication number 2138.

Funding

Financial support from Department of Biotechnology, Govt. of India (BT/PR/11001PBD/16/803/2008) is duly acknowledged.

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Authors and Affiliations

  1. Plant Virus Lab, Council of Scientific & Industrial Research, Institute of Himalayan Bioresource Technology, Palampur, HP, 176061, India

    Sunny Dhir & Vipin Hallan

  2. Amity Institute of Virology and Immunology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, 201313, India

    Sunny Dhir

  3. Plant Pathology Laboratory, Institute of Olive Tree, Subtropical Crops and Viticulture, ELGO-DIMITRA, Karamanlis Ave. 167, 73134, Chania, Greece

    Matthaios M. Mathioudakis

  4. Department of Virology and Bacteriology, Institute of Plant Protection-National Research Institute, ul. Wł. Węgorka 20, 60-318, Poznan, Poland

    Beata Hasiów-Jaroszewska

  5. Academy of Scientific and Innovative Research (AcSIR), New Delhi, India

    Sunny Dhir & Vipin Hallan

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  1. Sunny Dhir
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  2. Matthaios M. Mathioudakis
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Contributions

SD and VH conceived and designed the study. SD collected the samples and performed the experiments. MMM and BHJ performed data analysis. SD, MMM, BHJ and VH wrote the manuscript.

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Correspondence to Sunny Dhir or Vipin Hallan.

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Dhir, S., Mathioudakis, M.M., Hasiów-Jaroszewska, B. et al. Serological and molecular analysis indicates the presence of distinct viral genotypes of Apple stem pitting virus in India. 3 Biotech 11, 278 (2021). https://doi.org/10.1007/s13205-021-02798-5

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