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Fruit Fly Larval Survival in Picked and Unpicked Tomato Fruit of Differing Ripeness and Associated Gene Expression Patterns

SIMPLE SUMMARY: Tephritid fruit flies are major pests to a wide range of fruits and vegetables. Female flies lay their eggs into the fruit where the resultant larvae cause damage and yield loss. To replace pesticide-based controls with more sustainable management approaches, we need to develop new g...

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Autores principales: Roohigohar, Shirin, Clarke, Anthony R., Strutt, Francesca, van der Burg, Chloé A., Prentis, Peter J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9146954/
https://www.ncbi.nlm.nih.gov/pubmed/35621786
http://dx.doi.org/10.3390/insects13050451
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author Roohigohar, Shirin
Clarke, Anthony R.
Strutt, Francesca
van der Burg, Chloé A.
Prentis, Peter J.
author_facet Roohigohar, Shirin
Clarke, Anthony R.
Strutt, Francesca
van der Burg, Chloé A.
Prentis, Peter J.
author_sort Roohigohar, Shirin
collection PubMed
description SIMPLE SUMMARY: Tephritid fruit flies are major pests to a wide range of fruits and vegetables. Female flies lay their eggs into the fruit where the resultant larvae cause damage and yield loss. To replace pesticide-based controls with more sustainable management approaches, we need to develop new generation technologies. Enhancing fruit resistance is a promising alternative but it has received limited research attention. In this study, we examined larval survival and gene expression changes of B. tryoni larvae and tomato fruit while the fruits were in different picking statuses (unpicked vs. picked) and ripening stages (colour break vs. fully ripe). We assessed larval survival in two time points of 48 h and 120 h after inoculation. The fruit picking status and ripening stage had a significant effect on B. tryoni larval survival at 120 h. The gene expression patterns were not affected by picking status; however, insect detoxification genes and plant-induced defence genes were upregulated across the treatments. Overall, we anticipated the lack of conformity between larval survival and gene expression as a result of overlooked candidate genes or critical sampling time points. ABSTRACT: The larvae of frugivorous tephritid fruit flies feed within fruit and are global pests of horticulture. With the reduced use of pesticides, alternative control methods are needed, of which fruit resistance is one. In the current study, we explicitly tested for phenotypic evidence of induced fruit defences by running concurrent larval survival experiments with fruit on or off the plant, assuming that defence induction would be stopped or reduced by fruit picking. This was accompanied by RT-qPCR analysis of fruit defence and insect detoxification gene expression. Our fruit treatments were picking status (unpicked vs. picked) and ripening stage (colour break vs. fully ripe), our fruit fly was the polyphagous Bactrocera tryoni, and larval survival was assessed through destructive fruit sampling at 48 and 120 h, respectively. The gene expression study targeted larval and fruit tissue samples collected at 48 h and 120 h from picked and unpicked colour-break fruit. At 120 h in colour-break fruit, larval survival was significantly higher in the picked versus unpicked fruit. The gene expression patterns in larval and plant tissue were not affected by picking status, but many putative plant defence and insect detoxification genes were upregulated across the treatments. The larval survival results strongly infer an induced defence mechanism in colour-break tomato fruit that is stronger/faster in unpicked fruits; however, the gene expression patterns failed to provide the same clear-cut treatment effect. The lack of conformity between these results could be related to expression changes in unsampled candidate genes, or due to critical changes in gene expression that occurred during the unsampled periods.
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spelling pubmed-91469542022-05-29 Fruit Fly Larval Survival in Picked and Unpicked Tomato Fruit of Differing Ripeness and Associated Gene Expression Patterns Roohigohar, Shirin Clarke, Anthony R. Strutt, Francesca van der Burg, Chloé A. Prentis, Peter J. Insects Article SIMPLE SUMMARY: Tephritid fruit flies are major pests to a wide range of fruits and vegetables. Female flies lay their eggs into the fruit where the resultant larvae cause damage and yield loss. To replace pesticide-based controls with more sustainable management approaches, we need to develop new generation technologies. Enhancing fruit resistance is a promising alternative but it has received limited research attention. In this study, we examined larval survival and gene expression changes of B. tryoni larvae and tomato fruit while the fruits were in different picking statuses (unpicked vs. picked) and ripening stages (colour break vs. fully ripe). We assessed larval survival in two time points of 48 h and 120 h after inoculation. The fruit picking status and ripening stage had a significant effect on B. tryoni larval survival at 120 h. The gene expression patterns were not affected by picking status; however, insect detoxification genes and plant-induced defence genes were upregulated across the treatments. Overall, we anticipated the lack of conformity between larval survival and gene expression as a result of overlooked candidate genes or critical sampling time points. ABSTRACT: The larvae of frugivorous tephritid fruit flies feed within fruit and are global pests of horticulture. With the reduced use of pesticides, alternative control methods are needed, of which fruit resistance is one. In the current study, we explicitly tested for phenotypic evidence of induced fruit defences by running concurrent larval survival experiments with fruit on or off the plant, assuming that defence induction would be stopped or reduced by fruit picking. This was accompanied by RT-qPCR analysis of fruit defence and insect detoxification gene expression. Our fruit treatments were picking status (unpicked vs. picked) and ripening stage (colour break vs. fully ripe), our fruit fly was the polyphagous Bactrocera tryoni, and larval survival was assessed through destructive fruit sampling at 48 and 120 h, respectively. The gene expression study targeted larval and fruit tissue samples collected at 48 h and 120 h from picked and unpicked colour-break fruit. At 120 h in colour-break fruit, larval survival was significantly higher in the picked versus unpicked fruit. The gene expression patterns in larval and plant tissue were not affected by picking status, but many putative plant defence and insect detoxification genes were upregulated across the treatments. The larval survival results strongly infer an induced defence mechanism in colour-break tomato fruit that is stronger/faster in unpicked fruits; however, the gene expression patterns failed to provide the same clear-cut treatment effect. The lack of conformity between these results could be related to expression changes in unsampled candidate genes, or due to critical changes in gene expression that occurred during the unsampled periods. MDPI 2022-05-10 /pmc/articles/PMC9146954/ /pubmed/35621786 http://dx.doi.org/10.3390/insects13050451 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Roohigohar, Shirin
Clarke, Anthony R.
Strutt, Francesca
van der Burg, Chloé A.
Prentis, Peter J.
Fruit Fly Larval Survival in Picked and Unpicked Tomato Fruit of Differing Ripeness and Associated Gene Expression Patterns
title Fruit Fly Larval Survival in Picked and Unpicked Tomato Fruit of Differing Ripeness and Associated Gene Expression Patterns
title_full Fruit Fly Larval Survival in Picked and Unpicked Tomato Fruit of Differing Ripeness and Associated Gene Expression Patterns
title_fullStr Fruit Fly Larval Survival in Picked and Unpicked Tomato Fruit of Differing Ripeness and Associated Gene Expression Patterns
title_full_unstemmed Fruit Fly Larval Survival in Picked and Unpicked Tomato Fruit of Differing Ripeness and Associated Gene Expression Patterns
title_short Fruit Fly Larval Survival in Picked and Unpicked Tomato Fruit of Differing Ripeness and Associated Gene Expression Patterns
title_sort fruit fly larval survival in picked and unpicked tomato fruit of differing ripeness and associated gene expression patterns
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9146954/
https://www.ncbi.nlm.nih.gov/pubmed/35621786
http://dx.doi.org/10.3390/insects13050451
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