Phylogenomic and population genetics analyses of extant tomato yellow leaf curl virus strains on a global scale

Tomato yellow leaf curl virus (TYLCV) is a monopartite DNA virus with a genome size of ~ 2,800 base pairs. The virus belongs to the genus Begomovirus within the family Geminiviridae. Extant TYLCV strains are differentiated based on an established threshold of 94% genome-wide pairwise nucleotide iden...

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Main Authors: Wendy G. Marchant, Habibu Mugerwa, Saurabh Gautam, Hamed Al-Aqeel, Jane E. Polston, Gabriel Rennberger, Hugh Smith, Bill Turechek, Scott Adkins, Judith K. Brown, Rajagopalbabu Srinivasan
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Virology
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Online Access:https://www.frontiersin.org/articles/10.3389/fviro.2023.1221156/full
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author Wendy G. Marchant
Habibu Mugerwa
Saurabh Gautam
Hamed Al-Aqeel
Hamed Al-Aqeel
Jane E. Polston
Gabriel Rennberger
Gabriel Rennberger
Gabriel Rennberger
Hugh Smith
Bill Turechek
Scott Adkins
Judith K. Brown
Rajagopalbabu Srinivasan
author_facet Wendy G. Marchant
Habibu Mugerwa
Saurabh Gautam
Hamed Al-Aqeel
Hamed Al-Aqeel
Jane E. Polston
Gabriel Rennberger
Gabriel Rennberger
Gabriel Rennberger
Hugh Smith
Bill Turechek
Scott Adkins
Judith K. Brown
Rajagopalbabu Srinivasan
author_sort Wendy G. Marchant
collection DOAJ
description Tomato yellow leaf curl virus (TYLCV) is a monopartite DNA virus with a genome size of ~ 2,800 base pairs. The virus belongs to the genus Begomovirus within the family Geminiviridae. Extant TYLCV strains are differentiated based on an established threshold of 94% genome-wide pairwise nucleotide identity. The phylogenetic relationships, diversification mechanisms, including recombination, and extent of spread within and from the center of origin for TYLCV have been reported in previous studies. However, the evolutionary relationships among strains, strains’ distribution and genomic diversification, and genetic mechanisms shaping TYLCV strains’ evolution have not been re-evaluated to consider globally representative genome sequences in publicly available sequence database, including herein newly sequenced genomes from the U.S. and Middle East, respectively. In this study, full-length genome sequences for the extant strains and isolates of TYLCV (n=818) were downloaded from the GenBank database. All previously published genome sequences, and newly sequenced TYLCV genomes of TYLCV isolates from Kuwait and USA, determined herein (n=834), were subjected to recombination analysis. To remove the ‘phylogenetic noise’ imparted by interspecific recombination, the recombinant genomes were removed from the data set, and the remaining non-recombinant genome sequences (n=423) were subjected to population genetics and Bayesian analyses. Results of the phylogeographical analysis indicated that the type strain, TYLCV-Israel, and TYLCV-Mild strain, were globally distributed, spanning Africa, America, Asia, Australia/Oceania, Europe, and New Caledonia, while the other TYLCV strains were prevalent only throughout the Middle East. The results of Bayesian evolutionary (ancestral) analysis predicted that TYLCV-Israel represents the oldest, most recent common ancestor (MRCA) (41,795 years), followed by TYLCV-Mild at 39,808 years. These were closely followed by two Iranian strains viz., TYLCV-Kerman and TYLCV-Iran at 37,529 and 36,420 years, respectively. In contrast, the most recently evolving strains were TYLCV-Kuwait and TYLCV-Kahnooj at 12,445 and 298 years, respectively. Results of the neutrality test indicated that TYLCV-Israel and TYLCV-Mild populations are undergoing purifying selection and/or population expansion, although statistically significant selection was documented for only TYLCV-Israel, based on positive selection acting on five codons.
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spelling doaj.art-9b89c7f1ff5f4f558a936d0bbc98604e2023-07-25T21:05:31ZengFrontiers Media S.A.Frontiers in Virology2673-818X2023-07-01310.3389/fviro.2023.12211561221156Phylogenomic and population genetics analyses of extant tomato yellow leaf curl virus strains on a global scaleWendy G. Marchant0Habibu Mugerwa1Saurabh Gautam2Hamed Al-Aqeel3Hamed Al-Aqeel4Jane E. Polston5Gabriel Rennberger6Gabriel Rennberger7Gabriel Rennberger8Hugh Smith9Bill Turechek10Scott Adkins11Judith K. Brown12Rajagopalbabu Srinivasan13Department of Entomology, University of Georgia, Griffin, GA, United StatesDepartment of Entomology, University of Georgia, Griffin, GA, United StatesDepartment of Entomology, University of Georgia, Griffin, GA, United StatesDepartment of Plant Pathology, University of Florida, Gainesville, FL, United StatesKuwait Institute for Scientific Research, Environmental and Life Sciences Research Centre, Biotechnology Program, Kuwait, KuwaitKuwait Institute for Scientific Research, Environmental and Life Sciences Research Centre, Biotechnology Program, Kuwait, KuwaitGulf Coast Research and Education Center, University of Florida, Wimauma, FL, United StatesU.S. Horticultural Research Laboratory, USDA-Agricultural Research Service (ARS), Fort Pierce, FL, United StatesU.S. Vegetable Laboratory, USDA-Agricultural Research Service (ARS), Charleston, SC, United StatesGulf Coast Research and Education Center, University of Florida, Wimauma, FL, United StatesU.S. Horticultural Research Laboratory, USDA-Agricultural Research Service (ARS), Fort Pierce, FL, United StatesU.S. Horticultural Research Laboratory, USDA-Agricultural Research Service (ARS), Fort Pierce, FL, United StatesSchool of Plant Sciences, The University of Arizona, Tucson, AZ, United StatesDepartment of Entomology, University of Georgia, Griffin, GA, United StatesTomato yellow leaf curl virus (TYLCV) is a monopartite DNA virus with a genome size of ~ 2,800 base pairs. The virus belongs to the genus Begomovirus within the family Geminiviridae. Extant TYLCV strains are differentiated based on an established threshold of 94% genome-wide pairwise nucleotide identity. The phylogenetic relationships, diversification mechanisms, including recombination, and extent of spread within and from the center of origin for TYLCV have been reported in previous studies. However, the evolutionary relationships among strains, strains’ distribution and genomic diversification, and genetic mechanisms shaping TYLCV strains’ evolution have not been re-evaluated to consider globally representative genome sequences in publicly available sequence database, including herein newly sequenced genomes from the U.S. and Middle East, respectively. In this study, full-length genome sequences for the extant strains and isolates of TYLCV (n=818) were downloaded from the GenBank database. All previously published genome sequences, and newly sequenced TYLCV genomes of TYLCV isolates from Kuwait and USA, determined herein (n=834), were subjected to recombination analysis. To remove the ‘phylogenetic noise’ imparted by interspecific recombination, the recombinant genomes were removed from the data set, and the remaining non-recombinant genome sequences (n=423) were subjected to population genetics and Bayesian analyses. Results of the phylogeographical analysis indicated that the type strain, TYLCV-Israel, and TYLCV-Mild strain, were globally distributed, spanning Africa, America, Asia, Australia/Oceania, Europe, and New Caledonia, while the other TYLCV strains were prevalent only throughout the Middle East. The results of Bayesian evolutionary (ancestral) analysis predicted that TYLCV-Israel represents the oldest, most recent common ancestor (MRCA) (41,795 years), followed by TYLCV-Mild at 39,808 years. These were closely followed by two Iranian strains viz., TYLCV-Kerman and TYLCV-Iran at 37,529 and 36,420 years, respectively. In contrast, the most recently evolving strains were TYLCV-Kuwait and TYLCV-Kahnooj at 12,445 and 298 years, respectively. Results of the neutrality test indicated that TYLCV-Israel and TYLCV-Mild populations are undergoing purifying selection and/or population expansion, although statistically significant selection was documented for only TYLCV-Israel, based on positive selection acting on five codons.https://www.frontiersin.org/articles/10.3389/fviro.2023.1221156/fullGeminiviridaetomato-infecting begomovirusTYLCVstrainsancestral reconstruction
spellingShingle Wendy G. Marchant
Habibu Mugerwa
Saurabh Gautam
Hamed Al-Aqeel
Hamed Al-Aqeel
Jane E. Polston
Gabriel Rennberger
Gabriel Rennberger
Gabriel Rennberger
Hugh Smith
Bill Turechek
Scott Adkins
Judith K. Brown
Rajagopalbabu Srinivasan
Phylogenomic and population genetics analyses of extant tomato yellow leaf curl virus strains on a global scale
Frontiers in Virology
Geminiviridae
tomato-infecting begomovirus
TYLCV
strains
ancestral reconstruction
title Phylogenomic and population genetics analyses of extant tomato yellow leaf curl virus strains on a global scale
title_full Phylogenomic and population genetics analyses of extant tomato yellow leaf curl virus strains on a global scale
title_fullStr Phylogenomic and population genetics analyses of extant tomato yellow leaf curl virus strains on a global scale
title_full_unstemmed Phylogenomic and population genetics analyses of extant tomato yellow leaf curl virus strains on a global scale
title_short Phylogenomic and population genetics analyses of extant tomato yellow leaf curl virus strains on a global scale
title_sort phylogenomic and population genetics analyses of extant tomato yellow leaf curl virus strains on a global scale
topic Geminiviridae
tomato-infecting begomovirus
TYLCV
strains
ancestral reconstruction
url https://www.frontiersin.org/articles/10.3389/fviro.2023.1221156/full
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