Skip to main content

Advertisement

SpringerLink
Log in

Sequencing and assembly of small RNAs reveal the presence of several begomoviruses, potyviruses, badnaviruses and mastreviruses in the sweet potato leaf virome in Barbados

  • Original Article
  • Published:
Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Sweet potato [Ipomoea batatas (L.) Lam] is increasingly becoming an important food and industrial crop worldwide that is affected by over thirty viruses belonging to different virus families. Little is known about these viruses on the many local and commercial sweet potato cultivars in the Caribbean, including Barbados. Therefore, polymerase chain reaction (PCR) and small RNA sequencing and assembly (sRSA) were used to detect viruses in the sweet potato leaf virome in Barbados. The viruses detected by sRSA were mainly from two virus families in sweet potato: Geminiviridae (genus Begomovirus) and Caulimoviridae (genus Badnavirus). Together, these viruses accounted for more than 75% of the virus contigs found in the sweet potato leaf virome in Barbados. Although sweet potato feathery mottle virus (SPFMV, genus Potyvirus, family Potyviridae) was frequently detected by PCR in infected leaf samples, only 10% of the sequenced contigs matched to these viruses in the leaf virome. The results suggest the absence of the sweet potato virus disease complex (SPVD) in Barbados but reveal possibly new, severe single virus infections or emerging virus associations in the virome largely composed of begomoviruses, badnaviruses, potyviruses and mastreviruses previously unreported in sweet potato in the Caribbean.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Albuquerque LC, Inoue-Nagata AK, Pinheiro B, Resende RO, Moriones E, Navas-Castillo J (2012) Genetic diversity and recombination analysis of sweepoviruses from Brazil. Virol J 9:241

    Article  PubMed  PubMed Central  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Ateka EM, Barg E, Njeru RW, Lesemann D-E, Vettten HJ (2004) Further characterization of ‘sweet potato virus 2’: a distinct species of the genus Potyvirus. Arch Virol 149:225–239

    Article  CAS  PubMed  Google Scholar 

  • Chen YR, Zheng Y, Liu B, Zhong S, Giovannoni J, Fei Z (2012) A cost-effective method for Illumina small RNA-Seq library preparation using T4 RNA ligase 1 adenylated adapters. Plant Methods 8:41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark CA, Davis JA, Abad JA, Cuellar WJ, Fuentes S, Kreuze JF et al (2012) Sweetpotato viruses: 15 years of progress on understanding and managing complex diseases. Plant Dis 96(2):168–185. https://doi.org/10.1094/PDIS-07-11-0550

    Article  CAS  PubMed  Google Scholar 

  • Colinet D, Kummert J, Lepoivre P (1997) Evidence for the assignment of two strains of SPLV to the genus Potyvirus based on coat protein and 3′ non-coding region sequence data. Virus Res 49:91–100

    Article  CAS  PubMed  Google Scholar 

  • Cuellar WJ, Galvez M, Fuentes S, Tugume J, Kreuze J (2015) Synergistic interactions of begomoviruses with sweet potato chlorotic stunt virus (genus Crinivirus) in sweet potato (Ipomoea batatas L.). Mol Plant Pathol 16:459–471

    Article  CAS  PubMed  Google Scholar 

  • Gibson RW, Kreuze JF (2015) Degeneration in sweet potato due to viruses, virus cleaned planting material and reversion: a review. Plant Pathol 64:1–15. https://doi.org/10.1111/ppa.12273.

    Article  Google Scholar 

  • Gibson RW, Mpembe I, Alicai T, Carey EE, Mwanga ROM, Seal SE et al (1998) Symptoms, aetiology and serological analysis of sweet potato virus disease in Uganda. Plant Pathol 47:95–102. https://doi.org/10.1046/j.1365-3059.1998.00196.x

    Article  Google Scholar 

  • Gutiérrez DL, Fuentes S, Salazar LF (2003) Sweet potato virus disease (SPVD): distribution, incidence, and effect on sweet potato yield in Peru. Plant Dis 87:297–302

    Article  PubMed  Google Scholar 

  • Hassan I, Orillo A, Fiallo-Olive E, Briddon RW, Navas-Castillo J (2016) Infectivity, effects on helper viruses and whitefly transmission of the deltasatellites associated with sweepoviruses (genus Begomovirus, family Geminiviridae). Sci Rep 6:30204. https://doi.org/10.1038/srep30204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • James MS, Phillip MT, Fuentes S, Salazar LF (2003) A study on the cause of sweet potato virus disease in Barbados. Bridgetown. In: Proceedings of the Barbados National Agricultural Conference 2003: agricultural research and development: meeting the challenges of the 21st century. 10pp

  • Karyeija RF, Kreuze JF, Gibson RW, Valkonen JPT (2000) Synergistic interactions of a Potyvirus and a phloem-limited crinivirus in sweet potato plants. Virology 269:26–36

    Article  CAS  PubMed  Google Scholar 

  • Kashif M, Pietilä S, Artola K, Jones RAC, Tugume AK, Mäkinen V et al (2012) Detection of viruses in sweet potato from Honduras and Guatemala augmented by deep sequencing of small RNAs. Plant Dis 96(10):1430–1437. https://doi.org/10.1094/PDIS-03-12-0268-RE

    Article  CAS  PubMed  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Kokkinos CD, Clark CA (2006) Interactions among Sweet potato chlorotic stunt virus and different Potyviruses and Potyvirus strains infecting sweet potato in the United States. Plant Dis 90(10):1347–1352. https://doi.org/10.1094/PD-90-1347

    Article  CAS  PubMed  Google Scholar 

  • Kreuze JF, Perez A, Untiveros M, Quispe D, Fuentes S, Barker I et al (2009) Complete viral genome sequence and discovery of novel viruses by deep sequencing of small RNAs: a generic method for diagnosis, discovery and sequencing of viruses. Virology 388:1–7

    Article  CAS  PubMed  Google Scholar 

  • Li R, Salih S, Hurtt S (2004) Detection of Geminiviruses in sweet potato by polymerase chain reaction. Plant Dis 88(12):1347–1351

    Article  CAS  PubMed  Google Scholar 

  • Li R, Gao S, Hernandez AG, Wechter WP, Fei Z, Ling K-S (2012) Deep sequencing of small RNAs in tomato for virus and viroid identification and strain differentiation. PLoS One 7(5):e37127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lotrakul P, Valverde RA, Clark CA, Sim J, De La Torre R (1998) Detection of a Geminivirus infecting sweet potato in the United States. Plant Dis 82:1253–1257

    Article  CAS  PubMed  Google Scholar 

  • Lozano G, Trenado HP, Valverde RA, Navas-Castillo J (2009) Novel begomovirus species of recombinant nature in sweet potato (Ipomoea batatas) and Ipomoea indica: taxonomic and phylogenetic implications. J Gen Virol 90:2550–2562

    Article  CAS  PubMed  Google Scholar 

  • Mbanzibwa DR, Tairo F, Gwandu C, Kullaya A, Valkonen JPT (2011) First report of sweet potato symptomless virus 1 and sweet potato virus a in sweet potatoes in Tanzania. Plant Dis 95:224–225

    Article  CAS  PubMed  Google Scholar 

  • Rännäli M, Czekaj V, Jones RAC, Fletcher JD, Davis RI, Mu L et al (2008) Molecular genetic characterization of sweet potato virus G (SPVG) isolates from areas of the Pacific Ocean and southern Africa. Plant Dis 92(9):1313–1320. https://doi.org/10.1094/PDIS-92-9-1313

    Article  CAS  PubMed  Google Scholar 

  • Tairo F, Mukasa SB, Jones RAC, Kullaya A, Rubaihayo PR, Valkonen JPT (2005) Unravelling the genetic diversity of the three main viruses involved in sweet potato virus disease (SPVD), and its practical implications. Mol Plant Pathol 6:199–211

    Article  CAS  PubMed  Google Scholar 

  • Trenado HP, Oríllo AF, Márquez-Martín B, Moriones E, Navas-Castillo J (2011) Sweepoviruses cause disease in sweet potato and related Ipomoea spp.: fulfilling Koch’s postulates for a divergent group in the genus Begomovirus. PLoS One 6(11):e27329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tugume AK, Cuéllar WJ, Mukasa SB, Valkonen JPT (2010) Molecular genetic analysis of virus isolates from wild and cultivated plants demonstrates that East Africa is a hotspot for the evolution and diversification of Sweet potato feathery mottle virus. Mol Ecol 19:3139–3156

    Article  CAS  PubMed  Google Scholar 

  • Tugume AK, Mukasa SB, Valkonen JPT (2016) Mixed infections of four viruses, the incidence and phylogenetic relationships of sweet potato chlorotic fleck virus (Betaflexiviridae) isolates in wild species and Sweetpotatoes in Uganda and evidence of distinct isolates in East Africa. PLoS One 11(12):e0167769. https://doi.org/10.1371/journal.pone.0167769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Untiveros M, Fuentes S, Salazar LF (2007) Synergistic interaction of sweet potato chlorotic stunt virus (Crinivirus) with Carla-, Cucumo-, Ipomo-, and Potyviruses infecting sweet potato. Plant Dis 91:669–676

    Article  PubMed  Google Scholar 

  • Untiveros M, Fuentes S, Kreuze J (2008) Molecular variability of sweet potato feathery mottle virus and other potyviruses infecting sweet potato in Peru. Arch Virol 153:473–483

    Article  CAS  PubMed  Google Scholar 

  • Wasswa P, Otto B, Maruthi MN, Mukasa SB, Monger W, Gibson RW (2011) First identification of a sweet potato begomovirus (sweepovirus) in Uganda: characterization, detection and distribution. Plant Pathol 60(6):1030–1039. https://doi.org/10.1111/j.1365-3059.2011.02464.x.

    Article  CAS  Google Scholar 

  • Winter S, Körbler M, Köllner U (1997) Detection and differentiation of sweet potato closteroviruses by RT-PCR and single-strand conformation polymorphism. In: Dehne HW, Adam G, Diekmann M, Frahm J, Mauler-Machnik, van Halteren P (eds) Diagnosis and Identification of Plant Pathogens. Developments in Plant Pathology, vol 11. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-0043-1_104

  • Zheng Y, Gao S, Padmanabhan C, Li R, Galvez M, Gutierrez D et al (2017) VirusDetect: an automated pipeline for efficient virus discovery using deep sequencing of small RNAs. Virology 500:130–138. https://doi.org/10.1016/j.virol.2016.10.017

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded with support from The University of the West Indies and The Ministry of Agriculture, Food and Fisheries (MAFF), Plant Pathology Unit, Barbados. We also acknowledge the support provided by Carol Thomas of the Inter-American Institute for Cooperation on Agriculture (IICA), Barbados. We also thank those farmers who provided access to their fields for sample collection in Barbados. We thank Jan Kreuze for a critical review and suggestions to improve the manuscript.

Author information

Authors and Affiliations

  1. Faculty of Science and Technology, Department of Biological and Chemical Sciences, The University of the West Indies, Cave Hill Campus, PO Box 64, Bridgetown, BB11000, Barbados

    Angela T. Alleyne, Cara Cummins & Kherie Rowe

  2. Ministry of Agriculture and Food Security, Plant Pathology Section, Graeme Hall, Barbados

    Michael James

  3. Virology Laboratory, International Potato Center (CIP), Lima, Peru

    Dina L. Gutiérrez & Segundo Fuentes

Authors
  1. Angela T. Alleyne
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cara Cummins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kherie Rowe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael James
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dina L. Gutiérrez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Segundo Fuentes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angela T. Alleyne.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Table S1

(DOCX 20.6 kb)

Table S2

(DOCX 27 kb)

Table S3

(DOCX 19.8 kb)

Fig. S1

(PNG 1.91 mb)

High Resolution Image (TIF 55.6 mb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alleyne, A.T., Cummins, C., Rowe, K. et al. Sequencing and assembly of small RNAs reveal the presence of several begomoviruses, potyviruses, badnaviruses and mastreviruses in the sweet potato leaf virome in Barbados. J Plant Pathol 101, 339–347 (2019). https://doi.org/10.1007/s42161-018-00214-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42161-018-00214-1

Keywords

Search

Navigation