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Phylogenetics of tobacco rattle virus isolates from potato (Solanum tuberosum L.) in the USA: a multi-gene approach to evolutionary lineage

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Abstract

Tobacco rattle virus (TRV) is an important soil-borne virus of potato that is transmitted by stubby-root nematodes. TRV causes corky ringspot, a tuber disease of economic importance to potato production. Utilizing protein-coding regions of the whole genome and a range of computational tools, the genetic diversity, and population structure of TRV isolates from several potato-growing regions (Colorado, Idaho, Indiana, Minnesota, Nebraska, North Dakota, and Washington State) in the USA were determined. Phylogenetic analyses based on RNA2 nucleotide sequences, the coat protein (CP) and nematode transmission (2b) genes, showed geographical clustering of USA isolates with previously known American isolates, while European isolates grouped in a distinct cluster. This was corroborated by the observed genetic differentiation and infrequent gene flow between American and European isolates. Low genetic diversity was revealed among American isolates compared to European isolates. Phylogenetic clustering based on RNA1 genes (RdRp, RdRp-RT, and 1a) were all largely incongruent to that of 1b gene (virus suppressor of RNA silencing). This genetic incongruence suggested the influence of recombination. Furthermore, the RdRp, RdRp-RT, and 1a genes were predicted to be more conserved and under negative selection, while the 1b gene was less constrained. Different evolutionary lineages between TRV RNA1 and RNA2 genomic segments were revealed.

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Acknowledgements

We thank Dr. Prabu Gnanasekaran for a critical review of the manuscript. The research was supported by USDA-NIFA-SCRI Grant Number 2014-51181-22373, USDA National Institute of Food and Agriculture, Hatch project Accession #1016563 “Reducing the Impact of Pests and Diseases Affecting Washington Agriculture.” LM acknowledges support from a Fulbright fellowship and a 2016 Fulbright research grant award, Graduate Research Assistantships from the Graduate Program in Molecular Plant Sciences, and the Department of Plant Pathology at Washington State University (WSU), Pullman, WA, 99164, USA. LM also acknowledges a study-leave from the National University of Science and Technology, Bulawayo, Zimbabwe.

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Author notes

  1. Lindani Moyo

    Present address: Department of Plant Pathology, Stellenbosch University, Private Bag X1, Matieland, Stellenbosch, 7600, South Africa

Authors and Affiliations

  1. Department of Plant Pathology, Washington State University, Pullman, WA, 99164, USA

    Lindani Moyo, Gaurav Raikhy, Aflaq Hamid & Hanu R. Pappu

  2. Molecular Plant Sciences Graduate Program, Washington State University, Pullman, WA, 99164, USA

    Lindani Moyo & Hanu R. Pappu

  3. Department of Environmental Science and Health, National University of Science and Technology, PO Box AC939, Ascot, Bulawayo, Zimbabwe

    Lindani Moyo

  4. Department of Plant Pathology, North Dakota State University, Fargo, ND, 58108, USA

    Ipsita Mallik & Neil C. Gudmestad

  5. Section of Plant Pathology and Plant-Microbe Biology, School of Plant Science, Cornell University, Ithaca, NY, 14853, USA

    Stewart Gray

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Supplementary Information

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Supplementary file1 (TIF 72 kb)

Supplementary Figure S1 (a) The schematic representation of the genome organization of tobacco rattle virus (TRV) RNA1 (6791 nucleotides). Predicted open reading frames are represented by boxes. The sequences of different TRV isolates have sequence similarity both at 5′ and 3′ ends. Hence the primers used were based on previous studies of Crosslin (2010). The sequences of primers for complete RNA1 amplification are TRV_R1-F 5′-ATAAAACATTTCAATCCTTTGAACG-3′ and TRVR1-R 5′-GGGCGTAATAACGCTTACGTAG-3′. Along with these primers for complete genome amplification, a pair of primer was designed based on previous studies for amplification of 463bp fragment near the 3′ end of 16KDa gene of TRV RNA1. The primer pair is as follows: TRV_463-F 5′-CAGTCTATACACAGAAACAGA-3′ and TRVR1-R 5′-GACGTGTGTACTCAAGGGTT-3′. (b) Primers were designed to allow for amplification of TRV RNA1 as overlapping fragments, A-B (2.8 kb), C-D (1.6 kb) and E-F (2.3 kb). For the 2.8 kb fragment, primer pairs used are TRVR1-2F 5′-ATAAAACATTTCAATCCTTTGAACG-3′ and TRVRNA-2R 5′-TTGTCCAAGATCAACCTGTTAT-3′, for the 1.6 kb fragment primer pairs used are TRV1-3F 5′-ATAACAGGTTGATCTTGGACAA-3′ and TRV-3R TGGTTGCATAGCATCCAACTTG-3′ while for the 2.3 kb fragment primer pairs used are TRV1RNA-4F 5′-CAAGTTGGATGCTATGCAACCA-3′ and RNA-1R GGGCGTAACGCTTACGTAG-3′. Internal sequencing primers were designed to get the complete genome of TRV RNA1.

Supplementary file2 (TIF 302 kb)

Supplementary Figure S2 (a) Almost the complete sequence of RNA2 was amplified by using primer TR1 and 158 (I and J). Primer TR1 is 5′-GTTGGAGAACGCGGTAGA-3` and 158 is 5′-GGGCGTAATAACGCTTACG-3′. TR1 corresponds to the sequence at position 75–92 in RNA2 which is highly conserved in tobacco rattle virus (TRV) isolates (Schmitt et al., 1998); 158 is complementary to the 19 3′-terminal nucleotides of RNA2 of TRV isolates (MacFarlane, 1996). The forward primer at position G is R2-4 5′-ATAAAACATTGCACCWWTGGTGTTGC-3′ and reverse primer at position H is R2-3 5′-CGTAATAACGCTTACGTAGGCGAG-3′. MI-2 isolate (GenBank accession: GQ903772) is representative sequence showing complete RNA2 genome of TRV along with the locations of primers used in present studies. The 5′ region was found to be highly conserved among various TRV isolates when compared to the 3′ region. The internal sequencing primers were designed to sequence the complete amplicon of TRV RNA2. (b) The schematic diagram of RNA2 from different TRV isolates that were amplified and sequenced in the present studies.

Supplementary file3 (TIF 244 kb)

Supplementary Figure S3 Schematic representation of genome organization of tobacco rattle virus (TRV) RNA2 of six different isolates that are previously reported. Yellow colored boxes represent CP; Red color – 37 KDa/2b protein and blue colored boxes – 2c/18KDa/34KDa protein. Boxes with dash denote truncated ORFs. Downward arrow indicates start of sequence identical to the 3′-end of the RNA1. The sequences of different TRV isolates have sequence similarity both at 5′ and 3′ ends. Hence the primers used were based on previous studies of Crosslin (2010). The sequences of primers for complete RNA2 amplification is R2-4 5′-ATAAAACATTGCACCWWTGGTGTTGC-3′ and R2-3 5′-CGTAATAACGCTTACGTAGGCGAG-3′.

Supplementary file4 (DOCX 17 kb)

Supplementary Table S1 Evidence of breakpoints and recombination in tobacco rattle virus (TRV) RNA1 isolates.

Supplementary file5 (DOCX 17 kb)

Supplementary Table S2 Genetic differentiation and gene flow amongst tobacco rattle virus (TRV) populations for RNA1 and RNA2 gene sequences.

Supplementary file6 (DOCX 14 kb)

Supplementary Table S3 Neutrality tests in populations of tobacco rattle virus (TRV) based on RNA1 and RNA2 gene sequences.

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Moyo, L., Raikhy, G., Hamid, A. et al. Phylogenetics of tobacco rattle virus isolates from potato (Solanum tuberosum L.) in the USA: a multi-gene approach to evolutionary lineage. Virus Genes 58, 42–52 (2022). https://doi.org/10.1007/s11262-021-01875-4

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