New World Cactaceae Plants Harbor Diverse Geminiviruses
The family Cactaceae comprises a diverse group of typically succulent plants that are native to the American continent but have been introduced to nearly all other continents, predominantly for ornamental purposes. Despite their economic, cultural, and ecological importance, very little research has...
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MDPI AG
2021-04-01
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Online Access: | https://www.mdpi.com/1999-4915/13/4/694 |
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language |
English |
format |
Article |
sources |
DOAJ |
author |
Rafaela S. Fontenele Andrew M. Salywon Lucas C. Majure Ilaria N. Cobb Amulya Bhaskara Jesús A. Avalos-Calleros Gerardo R. Argüello-Astorga Kara Schmidlin Anthony Khalifeh Kendal Smith Joshua Schreck Michael C. Lund Matias Köhler Martin F. Wojciechowski Wendy C. Hodgson Raul Puente-Martinez Koenraad Van Doorslaer Safaa Kumari Kehinde A. Oyeniran Christian Vernière Denis Filloux Philippe Roumagnac Pierre Lefeuvre Simone G. Ribeiro Simona P. Kraberger Darren P. Martin Arvind Varsani |
spellingShingle |
Rafaela S. Fontenele Andrew M. Salywon Lucas C. Majure Ilaria N. Cobb Amulya Bhaskara Jesús A. Avalos-Calleros Gerardo R. Argüello-Astorga Kara Schmidlin Anthony Khalifeh Kendal Smith Joshua Schreck Michael C. Lund Matias Köhler Martin F. Wojciechowski Wendy C. Hodgson Raul Puente-Martinez Koenraad Van Doorslaer Safaa Kumari Kehinde A. Oyeniran Christian Vernière Denis Filloux Philippe Roumagnac Pierre Lefeuvre Simone G. Ribeiro Simona P. Kraberger Darren P. Martin Arvind Varsani New World Cactaceae Plants Harbor Diverse Geminiviruses Viruses Cactaceae <i>Geminiviridae</i> <i>Becurtovirus</i> recombination diversity |
author_facet |
Rafaela S. Fontenele Andrew M. Salywon Lucas C. Majure Ilaria N. Cobb Amulya Bhaskara Jesús A. Avalos-Calleros Gerardo R. Argüello-Astorga Kara Schmidlin Anthony Khalifeh Kendal Smith Joshua Schreck Michael C. Lund Matias Köhler Martin F. Wojciechowski Wendy C. Hodgson Raul Puente-Martinez Koenraad Van Doorslaer Safaa Kumari Kehinde A. Oyeniran Christian Vernière Denis Filloux Philippe Roumagnac Pierre Lefeuvre Simone G. Ribeiro Simona P. Kraberger Darren P. Martin Arvind Varsani |
author_sort |
Rafaela S. Fontenele |
title |
New World Cactaceae Plants Harbor Diverse Geminiviruses |
title_short |
New World Cactaceae Plants Harbor Diverse Geminiviruses |
title_full |
New World Cactaceae Plants Harbor Diverse Geminiviruses |
title_fullStr |
New World Cactaceae Plants Harbor Diverse Geminiviruses |
title_full_unstemmed |
New World Cactaceae Plants Harbor Diverse Geminiviruses |
title_sort |
new world cactaceae plants harbor diverse geminiviruses |
publisher |
MDPI AG |
series |
Viruses |
issn |
1999-4915 |
publishDate |
2021-04-01 |
description |
The family Cactaceae comprises a diverse group of typically succulent plants that are native to the American continent but have been introduced to nearly all other continents, predominantly for ornamental purposes. Despite their economic, cultural, and ecological importance, very little research has been conducted on the viral community that infects them. We previously identified a highly divergent geminivirus that is the first known to infect cacti. Recent research efforts in non-cultivated and asymptomatic plants have shown that the diversity of this viral family has been under-sampled. As a consequence, little is known about the effects and interactions of geminiviruses in many plants, such as cacti. With the objective to expand knowledge on the diversity of geminiviruses infecting cacti, we used previously acquired high-throughput sequencing results to search for viral sequences using BLASTx against a viral RefSeq protein database. We identified two additional sequences with similarity to geminiviruses, for which we designed abutting primers and recovered full-length genomes. From 42 cacti and five scale insects, we derived 42 complete genome sequences of a novel geminivirus species that we have tentatively named Opuntia virus 2 (OpV2) and 32 genomes of an Opuntia-infecting becurtovirus (which is a new strain of the spinach curly top Arizona virus species). Interspecies recombination analysis of the OpV2 group revealed several recombinant regions, in some cases spanning half of the genome. Phylogenetic analysis demonstrated that OpV2 is a novel geminivirus more closely related to viruses of the genus <i>Curtovirus</i>, which was further supported by the detection of three recombination events between curtoviruses and OpV2. Both OpV2 and Opuntia becurtoviruses were identified in mixed infections, which also included the previously characterized Opuntia virus 1. Viral quantification of the co-infected cactus plants compared with single infections did not show any clear trend in viral dynamics that might be associated with the mixed infections. Using experimental <i>Rhizobium</i>-mediated inoculations, we found that the initial accumulation of OpV2 is facilitated by co-infection with OpV1. This study shows that the diversity of geminiviruses that infect cacti is under-sampled and that cacti harbor diverse geminiviruses. The detection of the Opuntia becurtoviruses suggests spill-over events between viruses of cultivated species and native vegetation. The threat this poses to cacti needs to be further investigated. |
topic |
Cactaceae <i>Geminiviridae</i> <i>Becurtovirus</i> recombination diversity |
url |
https://www.mdpi.com/1999-4915/13/4/694 |
work_keys_str_mv |
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doaj-1a03507b4f3e46f19bcd1cdf2f9555b92021-04-16T23:06:30ZengMDPI AGViruses1999-49152021-04-011369469410.3390/v13040694New World Cactaceae Plants Harbor Diverse GeminivirusesRafaela S. Fontenele0Andrew M. Salywon1Lucas C. Majure2Ilaria N. Cobb3Amulya Bhaskara4Jesús A. Avalos-Calleros5Gerardo R. Argüello-Astorga6Kara Schmidlin7Anthony Khalifeh8Kendal Smith9Joshua Schreck10Michael C. Lund11Matias Köhler12Martin F. Wojciechowski13Wendy C. Hodgson14Raul Puente-Martinez15Koenraad Van Doorslaer16Safaa Kumari17Kehinde A. Oyeniran18Christian Vernière19Denis Filloux20Philippe Roumagnac21Pierre Lefeuvre22Simone G. Ribeiro23Simona P. Kraberger24Darren P. Martin25Arvind Varsani26The Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ 85287, USADesert Botanical Garden, Phoenix, AZ 85008, USAFlorida Museum of Natural History, University of Florida, Gainesville, FL 32611, USAThe Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ 85287, USAThe Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ 85287, USADivisión de Biología Molecular, Instituto Potosino de Investigación Científica y Tecnológica, A.C., Camino a la Presa de San José 2055, Lomas 4ta Secc, San Luis Potosi, San Luis Potosí 78216, MexicoDivisión de Biología Molecular, Instituto Potosino de Investigación Científica y Tecnológica, A.C., Camino a la Presa de San José 2055, Lomas 4ta Secc, San Luis Potosi, San Luis Potosí 78216, MexicoThe Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ 85287, USAThe Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ 85287, USAThe Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ 85287, USAThe Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ 85287, USAThe Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ 85287, USAPrograma de Pós-Graduação em Botânica, Universidade Federal do Rio Grande do Sul, Porto Alegre-RS 90040-060, BrazilSchool of Life Sciences, Arizona State University, Tempe, AZ 85287, USADesert Botanical Garden, Phoenix, AZ 85008, USADesert Botanical Garden, Phoenix, AZ 85008, USAUA Cancer Center, Department of Immunobiology, School of Animal and Comparative Biomedical Sciences, University of Arizona, Tucson, AZ 85721, USAInternational Center for Agricultural Research in the Dry Areas (ICARDA), Terbol Station, Beqa’a, Zahle, LebanonDepartment of Integrative Biomedical Sciences, Computational Biology Division, Institute of Infectious Diseases and Molecular Medicine, University of Cape Town, Observatory, Cape Town 7925, South AfricaCIRAD, UMR PHIM, 34090 Montpellier, FranceCIRAD, UMR PHIM, 34090 Montpellier, FranceCIRAD, UMR PHIM, 34090 Montpellier, FranceCIRAD, UMR PVBMT, F-97410 St. Pierre, FranceEmbrapa Recursos Genéticos e Biotecnologia, Brasília 70770-917, BrazilThe Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ 85287, USADepartment of Integrative Biomedical Sciences, Computational Biology Division, Institute of Infectious Diseases and Molecular Medicine, University of Cape Town, Observatory, Cape Town 7925, South AfricaThe Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ 85287, USAThe family Cactaceae comprises a diverse group of typically succulent plants that are native to the American continent but have been introduced to nearly all other continents, predominantly for ornamental purposes. Despite their economic, cultural, and ecological importance, very little research has been conducted on the viral community that infects them. We previously identified a highly divergent geminivirus that is the first known to infect cacti. Recent research efforts in non-cultivated and asymptomatic plants have shown that the diversity of this viral family has been under-sampled. As a consequence, little is known about the effects and interactions of geminiviruses in many plants, such as cacti. With the objective to expand knowledge on the diversity of geminiviruses infecting cacti, we used previously acquired high-throughput sequencing results to search for viral sequences using BLASTx against a viral RefSeq protein database. We identified two additional sequences with similarity to geminiviruses, for which we designed abutting primers and recovered full-length genomes. From 42 cacti and five scale insects, we derived 42 complete genome sequences of a novel geminivirus species that we have tentatively named Opuntia virus 2 (OpV2) and 32 genomes of an Opuntia-infecting becurtovirus (which is a new strain of the spinach curly top Arizona virus species). Interspecies recombination analysis of the OpV2 group revealed several recombinant regions, in some cases spanning half of the genome. Phylogenetic analysis demonstrated that OpV2 is a novel geminivirus more closely related to viruses of the genus <i>Curtovirus</i>, which was further supported by the detection of three recombination events between curtoviruses and OpV2. Both OpV2 and Opuntia becurtoviruses were identified in mixed infections, which also included the previously characterized Opuntia virus 1. Viral quantification of the co-infected cactus plants compared with single infections did not show any clear trend in viral dynamics that might be associated with the mixed infections. Using experimental <i>Rhizobium</i>-mediated inoculations, we found that the initial accumulation of OpV2 is facilitated by co-infection with OpV1. This study shows that the diversity of geminiviruses that infect cacti is under-sampled and that cacti harbor diverse geminiviruses. The detection of the Opuntia becurtoviruses suggests spill-over events between viruses of cultivated species and native vegetation. The threat this poses to cacti needs to be further investigated.https://www.mdpi.com/1999-4915/13/4/694Cactaceae<i>Geminiviridae</i><i>Becurtovirus</i>recombinationdiversity |