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Diversity of tomato-infecting begomoviruses and spatiotemporal dynamics of an endemic viral species of the Brazilian Atlantic rain forest biome

Abstract

Yield losses induced by a complex of begomoviruses are observed across all major tomato-producing areas in Brazil. Tomato severe rugose virus (ToSRV) is the most widespread begomovirus in the country. Conversely, tomato common mosaic virus (ToCmMV) displays a more restricted geographical distribution to areas associated with the Atlantic Rain Forest (ARF) biome, encompassing the States of Espírito Santo–ES, Minas Gerais–MG, and Rio de Janeiro–RJ. Here, we characterized 277 tomato-infecting isolates collected in fields located within the ARF biome from 2006 to 2018. ToSRV displayed the highest prevalence (n = 157), followed by ToCmMV (n = 95) and tomato interveinal chlorosis virus (n = 14). Four other begomoviruses were also detected, but with very low incidences. ToCmMV was the predominant begomovirus in the ARF biome up to 2014–2015 with very low ToSRV incidence. Subsequently, ToSRV became the most prevalent species in ES and RJ, but ToCmMV was still predominating in the “Zona da Mata” meso-region in MG. Due to the remarkable endemic distribution of ToCmMV, we carried out phylogeographical studies of this virus using information from all 28 available isolates with complete DNA–A sequences. The closest common ancestor of ToCmMV was more likely originated around Coimbra–MG area ≈ 25 years before the formal report of this viral species. So far, all surveys indicated tomatoes as the only natural hosts of ToCmMV with outbreaks occurring mainly (but not exclusively) in highland areas. ToSRV shows a more widespread incidence across both highland and lowland areas of the ARF biome.

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available at GenBank—NCBI public database (www.ncbi.nlm.nih.gov), including the ToCmMV isolates sequenced in the present work. These isolates were collected in six tomato–producing counties located either close to or within the Atlantic Rain Forest biome, encompassing the States of Espírito Santo–ES, Minas Gerais–MG, and Rio de Janeiro–RJ

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Acknowledgements

The authors would like to thank Antonio Francisco Costa for his technical support for processing the samples and Sanger dideoxy sequencing and Dr. Fernando Lucas Melo for his insightful contribution in the phylogeographical analyses.

Funding

This study was funded by FAP–DF, CAPES, CNPq, and Embrapa.

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MFD, MENF, LSB, and RCP-C conceived and designed the experiments; AR and HC performed sample collections; NANF carried out the initial organization and characterization of the collection of viral isolates; MFD performed the laboratory bench experiments; MFD and MENF performed the computational analysis of the data; MFD and LSB wrote the paper; LSB and RCP–C reviewed the manuscript.

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Correspondence to Rita C. Pereira-Carvalho.

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Duarte, M.F., Fonseca, M.E.N., Costa, H. et al. Diversity of tomato-infecting begomoviruses and spatiotemporal dynamics of an endemic viral species of the Brazilian Atlantic rain forest biome. Virus Genes 57, 83–93 (2021). https://doi.org/10.1007/s11262-020-01812-x

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Keywords

  • Geminiviridae
  • Begomovirus
  • Tomato severe rugose virus
  • Tomato common mosaic virus
  • Spatiotemporal dynamics