Ageing across the great divide: tissue transformation, organismal growth, and temperature shape telomere dynamics through the metamorphic transition

Burraco, P., Hernandez-Gonzalez, M., Metcalfe, N. B. and Monaghan, P. (2023) Ageing across the great divide: tissue transformation, organismal growth, and temperature shape telomere dynamics through the metamorphic transition. Proceedings of the Royal Society B: Biological Sciences, 290(1992), 20222448. (doi: 10.1098/rspb.2022.2448) (PMID:36750187)

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Abstract

Telomere attrition is considered a useful indicator of cellular and whole-organism ageing rate. While approximately 80% of animal species undergo metamorphosis that includes extensive tissue transformations (involving cell division, apoptosis, de-differentiation and de novo formation of stem cells), the effect on telomere dynamics is unknown. We measured telomeres in Xenopus laevis developing from larvae to adults under contrasting environmental temperatures. Telomere dynamics were linked to the degree of tissue transformation during development. Average telomere length in gut tissue increased dramatically during metamorphosis, when the gut shortens by 75% and epithelial cells de-differentiate into stem cells. In the liver (retained from larva) and hindlimb muscle (newly formed before metamorphosis), telomeres gradually shortened until adulthood, likely due to extensive cell division. Tail muscle telomere lengths were constant until tail resorption, and those in heart (retained from larva) showed no change over time. Telomere lengths negatively correlated with larval growth, but for a given growth rate, telomeres were shorter in cooler conditions, suggesting that growing in the cold is more costly. Telomere lengths were not related to post-metamorphic growth rate. Further research is now needed to understand whether telomere dynamics are a good indicator of ageing rate in species undergoing metamorphosis.

Item Type:Articles
Additional Information:P.B. was supported by Marie-Sklodowska-Curie Individual Fellowship 797879-METAGE—which also supported this study—and by Juan de la Cierva Incorporación IJC2020-044680-I (Spanish Ministry of Science and Innovation). N.B.M was supported by ERC Advanced Grant 834653 and P.M. by ERC Advanced Grant 101020037 under the European Union's Horizon 2020 research and innovation programme.
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Metcalfe, Professor Neil and Monaghan, Professor Pat and Burraco, Dr Pablo
Authors: Burraco, P., Hernandez-Gonzalez, M., Metcalfe, N. B., and Monaghan, P.
College/School:College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
Journal Name:Proceedings of the Royal Society B: Biological Sciences
Publisher:Royal Society of London
ISSN:0962-8452
ISSN (Online):1471-2954
Published Online:08 February 2023
Copyright Holders:Copyright © 2023 The Authors
First Published:First published in Proceedings of the Royal Society B: Biological Sciences 290(1992):20222448
Publisher Policy:Reproduced in accordance with the copyright policy of the publisher

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
305090MITOWILDNeil MetcalfeEuropean Commission (EC)834653Institute of Biodiversity, Animal Health and Comparative Medicine
312093InteragePatricia MonaghanEuropean Commission (EC)101020037Institute of Biodiversity, Animal Health and Comparative Medicine