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Using ‘sentinel’ plants to improve early detection of invasive plant pathogens

Infectious diseases of plants present an ongoing and increasing threat to international biosecurity, with wide-ranging implications. An important challenge in plant disease management is achieving early detection of invading pathogens, which requires effective surveillance through the implementation...

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Autores principales: Lovell-Read, Francesca A., Parnell, Stephen, Cunniffe, Nik J., Thompson, Robin N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9928126/
https://www.ncbi.nlm.nih.gov/pubmed/36730434
http://dx.doi.org/10.1371/journal.pcbi.1010884
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author Lovell-Read, Francesca A.
Parnell, Stephen
Cunniffe, Nik J.
Thompson, Robin N.
author_facet Lovell-Read, Francesca A.
Parnell, Stephen
Cunniffe, Nik J.
Thompson, Robin N.
author_sort Lovell-Read, Francesca A.
collection PubMed
description Infectious diseases of plants present an ongoing and increasing threat to international biosecurity, with wide-ranging implications. An important challenge in plant disease management is achieving early detection of invading pathogens, which requires effective surveillance through the implementation of appropriate monitoring programmes. However, when monitoring relies on visual inspection as a means of detection, surveillance is often hindered by a long incubation period (delay from infection to symptom onset) during which plants may be infectious but not displaying visible symptoms. ‘Sentinel’ plants–alternative susceptible host species that display visible symptoms of infection more rapidly–could be introduced to at-risk populations and included in monitoring programmes to act as early warning beacons for infection. However, while sentinel hosts exhibit faster disease progression and so allow pathogens to be detected earlier, this often comes at a cost: faster disease progression typically promotes earlier onward transmission. Here, we construct a computational model of pathogen transmission to explore this trade-off and investigate how including sentinel plants in monitoring programmes could facilitate earlier detection of invasive plant pathogens. Using Xylella fastidiosa infection in Olea europaea (European olive) as a current high profile case study, for which Catharanthus roseus (Madagascan periwinkle) is a candidate sentinel host, we apply a Bayesian optimisation algorithm to determine the optimal number of sentinel hosts to introduce for a given sampling effort, as well as the optimal division of limited surveillance resources between crop and sentinel plants. Our results demonstrate that including sentinel plants in monitoring programmes can reduce the expected prevalence of infection upon outbreak detection substantially, increasing the feasibility of local outbreak containment.
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spelling pubmed-99281262023-02-15 Using ‘sentinel’ plants to improve early detection of invasive plant pathogens Lovell-Read, Francesca A. Parnell, Stephen Cunniffe, Nik J. Thompson, Robin N. PLoS Comput Biol Research Article Infectious diseases of plants present an ongoing and increasing threat to international biosecurity, with wide-ranging implications. An important challenge in plant disease management is achieving early detection of invading pathogens, which requires effective surveillance through the implementation of appropriate monitoring programmes. However, when monitoring relies on visual inspection as a means of detection, surveillance is often hindered by a long incubation period (delay from infection to symptom onset) during which plants may be infectious but not displaying visible symptoms. ‘Sentinel’ plants–alternative susceptible host species that display visible symptoms of infection more rapidly–could be introduced to at-risk populations and included in monitoring programmes to act as early warning beacons for infection. However, while sentinel hosts exhibit faster disease progression and so allow pathogens to be detected earlier, this often comes at a cost: faster disease progression typically promotes earlier onward transmission. Here, we construct a computational model of pathogen transmission to explore this trade-off and investigate how including sentinel plants in monitoring programmes could facilitate earlier detection of invasive plant pathogens. Using Xylella fastidiosa infection in Olea europaea (European olive) as a current high profile case study, for which Catharanthus roseus (Madagascan periwinkle) is a candidate sentinel host, we apply a Bayesian optimisation algorithm to determine the optimal number of sentinel hosts to introduce for a given sampling effort, as well as the optimal division of limited surveillance resources between crop and sentinel plants. Our results demonstrate that including sentinel plants in monitoring programmes can reduce the expected prevalence of infection upon outbreak detection substantially, increasing the feasibility of local outbreak containment. Public Library of Science 2023-02-02 /pmc/articles/PMC9928126/ /pubmed/36730434 http://dx.doi.org/10.1371/journal.pcbi.1010884 Text en © 2023 Lovell-Read et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Lovell-Read, Francesca A.
Parnell, Stephen
Cunniffe, Nik J.
Thompson, Robin N.
Using ‘sentinel’ plants to improve early detection of invasive plant pathogens
title Using ‘sentinel’ plants to improve early detection of invasive plant pathogens
title_full Using ‘sentinel’ plants to improve early detection of invasive plant pathogens
title_fullStr Using ‘sentinel’ plants to improve early detection of invasive plant pathogens
title_full_unstemmed Using ‘sentinel’ plants to improve early detection of invasive plant pathogens
title_short Using ‘sentinel’ plants to improve early detection of invasive plant pathogens
title_sort using ‘sentinel’ plants to improve early detection of invasive plant pathogens
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9928126/
https://www.ncbi.nlm.nih.gov/pubmed/36730434
http://dx.doi.org/10.1371/journal.pcbi.1010884
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