Network Analysis of the Papaya Orchard Virome from Two Agroecological Regions of Chiapas, Mexico

ABSTRACT The study of complex ecological interactions, such as those among host, pathogen, and vector communities, can help to explain host ranges and the emergence of novel pathogens. We evaluated the viromes of papaya orchards, including weed and insect viromes, to identify common viruses in inten...

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Autores principales:	Ricardo I. Alcalá-Briseño, Kena Casarrubias-Castillo, Diana López-Ley, Karen A. Garrett, Laura Silva-Rosales
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	bipartite networks network analysis phytobiome plant viruses viral ecology viral metagenomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/15a1281199b949b092cbdd1b00d3cb42
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spelling	oai:doaj.org-article:15a1281199b949b092cbdd1b00d3cb422021-12-02T18:15:47ZNetwork Analysis of the Papaya Orchard Virome from Two Agroecological Regions of Chiapas, Mexico10.1128/mSystems.00423-192379-5077https://doaj.org/article/15a1281199b949b092cbdd1b00d3cb422020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00423-19https://doaj.org/toc/2379-5077ABSTRACT The study of complex ecological interactions, such as those among host, pathogen, and vector communities, can help to explain host ranges and the emergence of novel pathogens. We evaluated the viromes of papaya orchards, including weed and insect viromes, to identify common viruses in intensive production of papaya in the Pacific Coastal Plain and the Central Depression of Chiapas, Mexico. Samples of papaya cultivar Maradol, susceptible to papaya ringspot virus (PRSV), were categorized by symptoms by local farmers (papaya ringspot symptoms, non-PRSV symptoms, or asymptomatic). These analyses revealed the presence of 61 viruses, where only 4 species were shared among both regions, 16 showed homology to known viruses, and 36 were homologous with genera including Potyvirus, Comovirus, and Tombusvirus (RNA viruses) and Begomovirus and Mastrevirus (DNA viruses). We analyzed the network of associations between viruses and host-location combinations, revealing ecological properties of the network, such as an asymmetric nested pattern, and compared the observed network to null models of network association. Understanding the network structure informs management strategies, for example, revealing the potential role of PRSV in asymptomatic papaya and that weeds may be an important pathogen reservoir. We identify three key management implications: (i) each region may need a customized management strategy; (ii) visual assessment of papaya may be insufficient for PRSV, requiring diagnostic assays; and (iii) weed control within orchards may reduce the risk of virus spread to papaya. Network analysis advances understanding of host-pathogen interactions in the agroecological landscape. IMPORTANCE Virus-virus interactions in plants can modify host symptoms. As a result, disease management strategies may be unsuccessful if they are based solely on visual assessment and diagnostic assays for known individual viruses. Papaya ringspot virus is an important limiting factor for papaya production and likely has interactions with other viruses that are not yet known. Using high-throughput sequencing, we recovered known and novel RNA and DNA viruses from papaya orchards in Chiapas, Mexico, and categorized them by host and, in the case of papaya, symptom type: asymptomatic papaya, papaya with ringspot virus symptoms, papaya with nonringspot symptoms, weeds, and insects. Using network analysis, we demonstrated virus associations within and among host types and described the ecological community patterns. Recovery of viruses from weeds and asymptomatic papaya suggests the need for additional management attention. These analyses contribute to the understanding of the community structure of viruses in the agroecological landscape.Ricardo I. Alcalá-BriseñoKena Casarrubias-CastilloDiana López-LeyKaren A. GarrettLaura Silva-RosalesAmerican Society for Microbiologyarticlebipartite networksnetwork analysisphytobiomeplant virusesviral ecologyviral metagenomicsMicrobiologyQR1-502ENmSystems, Vol 5, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	bipartite networks network analysis phytobiome plant viruses viral ecology viral metagenomics Microbiology QR1-502
spellingShingle	bipartite networks network analysis phytobiome plant viruses viral ecology viral metagenomics Microbiology QR1-502 Ricardo I. Alcalá-Briseño Kena Casarrubias-Castillo Diana López-Ley Karen A. Garrett Laura Silva-Rosales Network Analysis of the Papaya Orchard Virome from Two Agroecological Regions of Chiapas, Mexico
description	ABSTRACT The study of complex ecological interactions, such as those among host, pathogen, and vector communities, can help to explain host ranges and the emergence of novel pathogens. We evaluated the viromes of papaya orchards, including weed and insect viromes, to identify common viruses in intensive production of papaya in the Pacific Coastal Plain and the Central Depression of Chiapas, Mexico. Samples of papaya cultivar Maradol, susceptible to papaya ringspot virus (PRSV), were categorized by symptoms by local farmers (papaya ringspot symptoms, non-PRSV symptoms, or asymptomatic). These analyses revealed the presence of 61 viruses, where only 4 species were shared among both regions, 16 showed homology to known viruses, and 36 were homologous with genera including Potyvirus, Comovirus, and Tombusvirus (RNA viruses) and Begomovirus and Mastrevirus (DNA viruses). We analyzed the network of associations between viruses and host-location combinations, revealing ecological properties of the network, such as an asymmetric nested pattern, and compared the observed network to null models of network association. Understanding the network structure informs management strategies, for example, revealing the potential role of PRSV in asymptomatic papaya and that weeds may be an important pathogen reservoir. We identify three key management implications: (i) each region may need a customized management strategy; (ii) visual assessment of papaya may be insufficient for PRSV, requiring diagnostic assays; and (iii) weed control within orchards may reduce the risk of virus spread to papaya. Network analysis advances understanding of host-pathogen interactions in the agroecological landscape. IMPORTANCE Virus-virus interactions in plants can modify host symptoms. As a result, disease management strategies may be unsuccessful if they are based solely on visual assessment and diagnostic assays for known individual viruses. Papaya ringspot virus is an important limiting factor for papaya production and likely has interactions with other viruses that are not yet known. Using high-throughput sequencing, we recovered known and novel RNA and DNA viruses from papaya orchards in Chiapas, Mexico, and categorized them by host and, in the case of papaya, symptom type: asymptomatic papaya, papaya with ringspot virus symptoms, papaya with nonringspot symptoms, weeds, and insects. Using network analysis, we demonstrated virus associations within and among host types and described the ecological community patterns. Recovery of viruses from weeds and asymptomatic papaya suggests the need for additional management attention. These analyses contribute to the understanding of the community structure of viruses in the agroecological landscape.
format	article
author	Ricardo I. Alcalá-Briseño Kena Casarrubias-Castillo Diana López-Ley Karen A. Garrett Laura Silva-Rosales
author_facet	Ricardo I. Alcalá-Briseño Kena Casarrubias-Castillo Diana López-Ley Karen A. Garrett Laura Silva-Rosales
author_sort	Ricardo I. Alcalá-Briseño
title	Network Analysis of the Papaya Orchard Virome from Two Agroecological Regions of Chiapas, Mexico
title_short	Network Analysis of the Papaya Orchard Virome from Two Agroecological Regions of Chiapas, Mexico
title_full	Network Analysis of the Papaya Orchard Virome from Two Agroecological Regions of Chiapas, Mexico
title_fullStr	Network Analysis of the Papaya Orchard Virome from Two Agroecological Regions of Chiapas, Mexico
title_full_unstemmed	Network Analysis of the Papaya Orchard Virome from Two Agroecological Regions of Chiapas, Mexico
title_sort	network analysis of the papaya orchard virome from two agroecological regions of chiapas, mexico
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/15a1281199b949b092cbdd1b00d3cb42
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Network Analysis of the Papaya Orchard Virome from Two Agroecological Regions of Chiapas, Mexico

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