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Characterisation of turnip mosaic virus isolates reveals high genetic variability and occurrence of pathotype 1 in Brazil

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Abstract

Turnip mosaic virus (TuMV) infects many plant species, being the only potyvirus able to infect brassicas. TuMV isolates have been classified into 12 pathotypes according to symptoms induced in lines of Brassica napus, and molecularly clustered into six lineages (basal-B, basal-BR, Asian-BR, world-B, Iranian and OMs). Despite being considered one of the most important viruses infecting brassicas worldwide, there is little information on this virus in the Neotropical region. Aiming to fill in this gap and advance knowledge on occurrence, genetic variability, and biological aspects of TuMV in Brazil, 40 isolates were identified and characterised. Five of these isolates were selected to determine their host range, sequence their genomes, and for phylogenetic, recombination and diversity analyses. Mechanical inoculations performed on plant species from 10 families showed differences in symptom expression among isolates. Inoculations of 13 TuMV isolates in B. napus lines revealed occurrence only of the pathotype 1. According to phylogenetic analyses of the coat protein, TuMV Brazilian isolates clustered into the groups: world-B (subgroups world-B2 and world-B3) and basal-BR. In the latter, there was a formation of a subclade named Brazilian subgroup composed by 31 Brazilian TuMV isolates. Intralineage and interlineage recombination events of world-B, basal-B and basal-BR suggest that Brazilian TuMV isolates had a European origin. Our diversity analysis suggest that a strong negative selection is acting on polyprotein coding region. We confirmed that Brazilian TuMV isolates showed high variability, which together with their ability to infect wild brassicas and to circumvent resistance genes highlight their genetic and epidemiological potential in causing damages in cultivated species of brassicas and other crops in Brazil.

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Acknowledgements

We are grateful to Alyne de Fátima Ramos (Instituto Biológico, Brazil) for technical assistance.

Funding

The research conducted in ME’s laboratory was supported by “Fundação de Amparo à Pesquisa do Estado de São Paulo”, FAPESP (Grants: 2014/22594–2; 2015/50076–9; 2018/17287–4). The research conducted in EWK’s laboratory was supported by FAPESP (Grant: 2017/18910–4). This study was financed in part by the “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior”, CAPES - Brazil - Finance Code 001. LKR was recipient of a CAPES Ph.D. fellowship. EWK, RH and ME are supported by a CNPq research fellowship. JAW’s contributions were funded by the University of Warwick’s Brazil Partnership Fund, FAPESP-Warwick Joint Fund, with support from Santander (project codes 09LFAA00 and LFSP02).

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Authors and Affiliations

  1. Instituto Biológico, Centro de Pesquisa de Sanidade Vegetal, Av. Conselheiro Rodrigues Alves, 1252, CEP, São Paulo, SP, 04014-002, Brazil

    Leilane Karam Rodrigues, Alexandre Levi Rodrigues Chaves, Ricardo Harakava & Marcelo Eiras

  2. Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, CEP, Piracicaba, SP, 13418-400, Brazil

    Elliot Watanabe Kitajima

  3. Universidade Federal do Paraná, CEP, Curitiba, PR, 80060-000, Brazil

    Renata Faier Calegario

  4. Sakata Seed Sudamerica, CEP, Bragança Paulista, SP, 12906-840, Brazil

    Katia Regiane Brunelli

  5. Universidade do Estado de Santa Catarina, CEP, Lages, SC, 88520-000, Brazil

    Fabio Nascimento da Silva

  6. School of Life Sciences, University of Warwick, Coventry, CV35 9EF, UK

    John Anthony Walsh

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  1. Leilane Karam Rodrigues
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Correspondence to Marcelo Eiras.

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Supplementary Information

Supplementary Fig. S1

Detection of turnip mosaic virus (TuMV) isolates by RT-PCR. Electrophoresis in 1.2% agarose gel of the amplicons using primers (CI-F/CI-R) for the cylindrical inclusion (CI) TuMV genomic region, with expected size of 700 bp (above); and amplicons using primers (CP-F/CP-R) for TuMV coat protein (CP) genomic region amplification, with expected size of 986 bp (below). The lanes T06, T22, T31, T48 and T61 correspond to the five Brazilian TuMV isolates sequenced in this work (Supplementary Table S1). C+: TuMV-infected Chinese cabbage (Brassica rapa ssp. pekinensis). C-: healthy Chinese cabbage plant. The lanes to the left of the agarose gel correspond to the molecular weight marker (DNA 1 kb ladder, Promega, Madison City, WI, USA) (JPG 395 kb)

Supplementary Fig. S2

Scheme of the turnip mosaic virus (TuMV) genome with the indication (arrows) of the cleavage sites in the polyprotein (post-translational processing), which give rise to the viral proteins, with their respective amino acids for the five isolates (T06, T22, T31, T48, T61) fully sequenced in this work. Methionine (M); Phenylalanine (F); Tyrosine (Y); Serine (S); Glycine (G); Glutamine (Q); Threonine (T); Asparagine (N); Alanine (A); Glutamic acid (E); Tryptophan (W); Leucine (L) and Lysine (K). (PNG 132 kb)

Supplementary Fig. S3

Average pairwise number of nucleotide differences per site (nucleotide diversity, π) calculated on a sliding window across the polyprotein of turnip mosaic virus (TuMV). (A) “World” dataset comprising isolates from Australia (04), Belgium (01), Brazil (06), Canada (01), China (4), Croatia (01), Czech Republic (02), Denmark (01), France (01), Germany (11), Greece (03), Hungary (01), Iran (02), Israel (01), Italy (07), Japan (07), Kenya (01), Mexico (01), New Zealand (01), Poland (02), Portugal (01), Russia (01), South Korea (02), Spain (01), Turkey (01), United Kingdom (06) and United States of America (4). (B) Brazilian dataset including six isolates. The isolates of TuMV used for these analyses with their respective access codes at GenBank can be accessed in the Supplementary Table S1 and S2. (PNG 1040 kb)

High Resolution Image (TIF 441 kb)

Supplementary Fig. S4

Mean pairwise number of nucleotide differences per site (nucleotide diversity, π) at synonymous (A) and non-synonymous (B) sites calculated for three regions (5′-terminal, central and 3′ terminal) of the polyprotein of turnip mosaic virus (TuMV) isolates from Brazil, Australia, China, Germany, Italy, Japan, United Kingdom (UK) and United States of America (USA). (PNG 281 kb)

High Resolution Image (TIF 187 kb)

Supplementary Table S1

(DOCX 17 kb)

Supplementary Table S2

(DOCX 13 kb)

Supplementary Table S3

(DOCX 26 kb)

Supplementary Table S4

(DOCX 19 kb)

Supplementary Table S5

(DOCX 18 kb)

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Rodrigues, L.K., Chaves, A.L.R., Kitajima, E.W. et al. Characterisation of turnip mosaic virus isolates reveals high genetic variability and occurrence of pathotype 1 in Brazil. Eur J Plant Pathol 160, 883–900 (2021). https://doi.org/10.1007/s10658-021-02291-y

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