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Mosaic genome evolution and phylogenetics of Chrysodeixis includens nucleopolyhedrovirus (ChinNPV) and virulence of seven new isolates from the Brazilian states of Minas Gerais and Mato Grosso

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Abstract

In a comparative analysis of genome sequences from isolates of the baculovirus Chrysodeixis includens nucleopolyhedrovirus (ChinNPV) from Brazil and Guatemala, we identified a subset of isolates possessing chimeric genomes. We identified six distinct phylogenetically incongruous regions (PIRs) dispersed in the genomes, of between 279 and 3345 bp in length. The individual PIRs possessed high sequence similarity among the affected ChinNPV isolates but varied in coverage in some instances. The donor for four of the PIRs implicated in horizontal gene transfer (HGT) was identified as Trichoplusia ni single nucleopolyhedrovirus (TnSNPV), an alphabaculovirus closely related to ChinNPV, or another unknown but closely related virus. BLAST searches of the other two PIRs returned only ChinNPV sequences, but HGT from an unknown donor baculovirus cannot be excluded. Although Chrysodeixis includens and Trichoplusia ni are frequently co-collected from soybean fields in Brazil, pathogenicity data suggest that natural coinfection of C. includens larvae with ChinNPV and TnSNPV is probably uncommon. Additionally, since the chimeric ChinNPV genomes with tracts of TnSNPV sequence were restricted to a single monophyletic lineage of closely related isolates, a model of progressive restoration of the native DNA sequence by recombination with ChinNPV possessing a fully or partially non-chimeric genome is reasonable. However, multiple independent HGT from TnSNPV to ChinNPV during the evolution of these isolates cannot be excluded. Mortality data suggest that the ChinNPV isolates with chimeric genomes are not significantly different in pathogenicity towards C. includens when compared to most other ChinNPV isolates. Exclusion of the PIRs prior to phylogenetic analysis had a large impact on the topology of part of the maximum-likelihood tree, revealing a homogenous clade of three isolates (IB, IC and ID) from Paraná state in Brazil collected in 2006, together with an isolate from Guatemala collected in 1972 (IA), comprising the lineage uniquely affected by HGT from TnSNPV. The other 10 Brazilian ChinNPV isolates from Paraná, Mato Grosso, and Minas Gerais states showed higher variability, where only three isolates from Paraná state formed a monophyletic group correlating with geographical origin.

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Acknowledgements

This work was supported in part from Fundação de Apoio a Pesquisa do Distrito Federal (FAPDF) grant number 193.001532/2016 to BMR/Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and grant number 305756/2017-6 to BMR/Universidade de Brasília (UnB)/Embrapa Recursos Genéticos e Biotecnologia. Further funding was provided by Embrapa and grant 193.001531/2016-PRONEX (Programa de Apoio a Núcleos de Excelência). The authors also wish to thank Zilda M.A. Ribeiro for laboratory support.

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MEBC contributed to the study conception, funding acquisition and design. BMR also contributed to funding acquisition. Material preparation, data collection and analysis were performed by LAVMS, SRC and PWI. The first draft of the manuscript was written by PWI, MEBC and BMR and all authors read and approved the final manuscript.

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Correspondence to Peter W. Inglis.

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Supplementary file1 Fig. S1 Mauve collinearity plot of ChinNPV genomes along with TnSNPV and ChchSNPV genomes (TIF 1905 kb)

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Supplementary file2 Fig. S2 Midpoint-rooted ML tree of ChinNPV, TnSNPV and ChchSNPV genome sequences. The tree was calculated in IQTREE using an unpartitioned TVM+F+R5 model, selected as optimal according to BIC. Support values given above branches are ultrafast bootstrap percentages. GenBank numbers of genome sequences are given in Tables 3 and 4 (EPS 1239 kb)

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Supplementary file3 Fig. S3 Midpoint-rooted ML tree of ChinNPV, TnSNPV and ChchSNPV genome sequences, with phylogenetically incongruent regions identified among ChinNPV isolates deleted. The tree was calculated in IQTREE using an unpartitioned TVM+F+R6 model, selected as optimal according to BIC. Support values given above branches are ultrafast bootstrap percentages. GenBank numbers of genome sequences are given in Tables 3 and 4 (EPS 1152 kb)

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Inglis, P.W., Santos, L.A.V.M., Craveiro, S.R. et al. Mosaic genome evolution and phylogenetics of Chrysodeixis includens nucleopolyhedrovirus (ChinNPV) and virulence of seven new isolates from the Brazilian states of Minas Gerais and Mato Grosso. Arch Virol 166, 125–138 (2021). https://doi.org/10.1007/s00705-020-04858-2

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  • DOI: https://doi.org/10.1007/s00705-020-04858-2

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