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New World Cactaceae Plants Harbor Diverse Geminiviruses

The Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ 85287, USA
School of Life Sciences, Arizona State University, Tempe, AZ 85287, USA
Desert Botanical Garden, Phoenix, AZ 85008, USA
Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA
The University of British Columbia, Vancouver, BC V6T 1Z4, Canada
School of Behavioral and Brain Sciences, University of Texas at Dallas, 800 W Campbell Rd, Richardson, TX 75080, USA
División 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, Mexico
Programa de Pós-Graduação em Botânica, Universidade Federal do Rio Grande do Sul, Porto Alegre-RS 90040-060, Brazil
UA Cancer Center, Department of Immunobiology, School of Animal and Comparative Biomedical Sciences, University of Arizona, Tucson, AZ 85721, USA
International Center for Agricultural Research in the Dry Areas (ICARDA), Terbol Station, Beqa’a, Zahle, Lebanon
Department of Integrative Biomedical Sciences, Computational Biology Division, Institute of Infectious Diseases and Molecular Medicine, University of Cape Town, Observatory, Cape Town 7925, South Africa
CIRAD, UMR PHIM, 34090 Montpellier, France
Plant Health Institute, University Montpellier, INRAE, CIRAD, 34090 Montpellier, France
CIRAD, UMR PVBMT, F-97410 St. Pierre, France
Embrapa Recursos Genéticos e Biotecnologia, Brasília 70770-917, Brazil
Center for Evolution and Medicine, Arizona State University, Tempe, AZ 85287, USA
Structural Biology Research Unit, Department of Clinical Laboratory Sciences, University of Cape Town, Cape Town 7925, South Africa
Author to whom correspondence should be addressed.
Academic Editor: Jan Frederik Kreuze
Viruses 2021, 13(4), 694;
Received: 15 March 2021 / Revised: 11 April 2021 / Accepted: 13 April 2021 / Published: 16 April 2021
(This article belongs to the Special Issue Plant Virus Surveillance and Metagenomics)
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 Curtovirus, 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 Rhizobium-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. View Full-Text
Keywords: Cactaceae; Geminiviridae; Becurtovirus; recombination; diversity Cactaceae; Geminiviridae; Becurtovirus; recombination; diversity
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MDPI and ACS Style

Fontenele, R.S.; Salywon, A.M.; Majure, L.C.; Cobb, I.N.; Bhaskara, A.; Avalos-Calleros, J.A.; Argüello-Astorga, G.R.; Schmidlin, K.; Khalifeh, A.; Smith, K.; Schreck, J.; Lund, M.C.; Köhler, M.; Wojciechowski, M.F.; Hodgson, W.C.; Puente-Martinez, R.; Van Doorslaer, K.; Kumari, S.; Oyeniran, K.A.; Vernière, C.; Filloux, D.; Roumagnac, P.; Lefeuvre, P.; Ribeiro, S.G.; Kraberger, S.P.; Martin, D.P.; Varsani, A. New World Cactaceae Plants Harbor Diverse Geminiviruses. Viruses 2021, 13, 694.

AMA Style

Fontenele RS, Salywon AM, Majure LC, Cobb IN, Bhaskara A, Avalos-Calleros JA, Argüello-Astorga GR, Schmidlin K, Khalifeh A, Smith K, Schreck J, Lund MC, Köhler M, Wojciechowski MF, Hodgson WC, Puente-Martinez R, Van Doorslaer K, Kumari S, Oyeniran KA, Vernière C, Filloux D, Roumagnac P, Lefeuvre P, Ribeiro SG, Kraberger SP, Martin DP, Varsani A. New World Cactaceae Plants Harbor Diverse Geminiviruses. Viruses. 2021; 13(4):694.

Chicago/Turabian Style

Fontenele, Rafaela S., 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, and Arvind Varsani. 2021. "New World Cactaceae Plants Harbor Diverse Geminiviruses" Viruses 13, no. 4: 694.

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