Single torradovirus infections explain the mysterious cassava frogskin disease in the Americas

Abstract Cassava frogskin disease (CFSD) emerged in the Americas in the 1970s, but its causal agent has to date remained a mystery. The clonal propagation of cassava, high incidence of mixed infections, unknown alternative hosts, and root symptoms taking two or more crop cycles to develop, have made...

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Main Authors: Jenyfer Jimenez, Sara Caicedo, Juan M. Pardo, Alejandra Gil-Ordóñez, Robert Alvarez-Quinto, Dimitre Mollov, Wilmer J. Cuellar
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-81142-2
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author Jenyfer Jimenez
Sara Caicedo
Juan M. Pardo
Alejandra Gil-Ordóñez
Robert Alvarez-Quinto
Dimitre Mollov
Wilmer J. Cuellar
author_facet Jenyfer Jimenez
Sara Caicedo
Juan M. Pardo
Alejandra Gil-Ordóñez
Robert Alvarez-Quinto
Dimitre Mollov
Wilmer J. Cuellar
author_sort Jenyfer Jimenez
collection DOAJ
description Abstract Cassava frogskin disease (CFSD) emerged in the Americas in the 1970s, but its causal agent has to date remained a mystery. The clonal propagation of cassava, high incidence of mixed infections, unknown alternative hosts, and root symptoms taking two or more crop cycles to develop, have made it difficult to identify the causal agent. Consequently, most studies on CFSD have produced a catalogue of pathogens occurring in affected plants. Using a sentinel approach, we captured single-pathogen infections in fields with high incidence of root symptoms. Eight months after being exposed to CFSD, we detected < 6.9% incidence of root symptoms in sentinel plants. Plants were then propagated and transferred to a screenhouse for a second infection cycle and storage root development. Interestingly, molecular diagnostics did not identify an association with phytoplasma or reovirids—pathogens historically reported in CFSD-infected plants—but indicated that single-infections by torradoviruses were sufficient to cause the disease. Further analysis by high-throughput sequencing confirmed the presence of torradoviruses in symptomatic roots and allowed unveiling the occurrence of a second torradovirus species in farmers’ fields in Colombia. These new findings should support early interception of infected planting material, development of cassava seed certification standards, breeding and screening for resistance programs, and ultimately significantly reduce the impact of CFSD in cassava.
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spelling doaj-art-02d454ac9bb94fc087b0457713a10dd22024-12-01T12:22:03ZengNature PortfolioScientific Reports2045-23222024-11-0114111210.1038/s41598-024-81142-2Single torradovirus infections explain the mysterious cassava frogskin disease in the AmericasJenyfer Jimenez0Sara Caicedo1Juan M. Pardo2Alejandra Gil-Ordóñez3Robert Alvarez-Quinto4Dimitre Mollov5Wilmer J. Cuellar6Virology and Crop Protection Laboratory, Cassava Program, International Center for Tropical Agriculture (CIAT)Virology and Crop Protection Laboratory, Cassava Program, International Center for Tropical Agriculture (CIAT)Virology and Crop Protection Laboratory, Cassava Program, International Center for Tropical Agriculture (CIAT)Virology and Crop Protection Laboratory, Cassava Program, International Center for Tropical Agriculture (CIAT)Department of Plant Pathology, University of MinnesotaPest Exclusion and Import Programs, USDA APHIS Plant Protection and QuarantineVirology and Crop Protection Laboratory, Cassava Program, International Center for Tropical Agriculture (CIAT)Abstract Cassava frogskin disease (CFSD) emerged in the Americas in the 1970s, but its causal agent has to date remained a mystery. The clonal propagation of cassava, high incidence of mixed infections, unknown alternative hosts, and root symptoms taking two or more crop cycles to develop, have made it difficult to identify the causal agent. Consequently, most studies on CFSD have produced a catalogue of pathogens occurring in affected plants. Using a sentinel approach, we captured single-pathogen infections in fields with high incidence of root symptoms. Eight months after being exposed to CFSD, we detected < 6.9% incidence of root symptoms in sentinel plants. Plants were then propagated and transferred to a screenhouse for a second infection cycle and storage root development. Interestingly, molecular diagnostics did not identify an association with phytoplasma or reovirids—pathogens historically reported in CFSD-infected plants—but indicated that single-infections by torradoviruses were sufficient to cause the disease. Further analysis by high-throughput sequencing confirmed the presence of torradoviruses in symptomatic roots and allowed unveiling the occurrence of a second torradovirus species in farmers’ fields in Colombia. These new findings should support early interception of infected planting material, development of cassava seed certification standards, breeding and screening for resistance programs, and ultimately significantly reduce the impact of CFSD in cassava.https://doi.org/10.1038/s41598-024-81142-2CassavaEmergent diseaseHigh-throughput sequencingDisease diagnostics
spellingShingle Jenyfer Jimenez
Sara Caicedo
Juan M. Pardo
Alejandra Gil-Ordóñez
Robert Alvarez-Quinto
Dimitre Mollov
Wilmer J. Cuellar
Single torradovirus infections explain the mysterious cassava frogskin disease in the Americas
Scientific Reports
Cassava
Emergent disease
High-throughput sequencing
Disease diagnostics
title Single torradovirus infections explain the mysterious cassava frogskin disease in the Americas
title_full Single torradovirus infections explain the mysterious cassava frogskin disease in the Americas
title_fullStr Single torradovirus infections explain the mysterious cassava frogskin disease in the Americas
title_full_unstemmed Single torradovirus infections explain the mysterious cassava frogskin disease in the Americas
title_short Single torradovirus infections explain the mysterious cassava frogskin disease in the Americas
title_sort single torradovirus infections explain the mysterious cassava frogskin disease in the americas
topic Cassava
Emergent disease
High-throughput sequencing
Disease diagnostics
url https://doi.org/10.1038/s41598-024-81142-2
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