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Genome damage accumulated in seed ageing leads to plant genome instability and growth inhibition

Successful germination and seedling establishment are important determinants of crop yields and plant survival in natural environments. Germination potential is compromised by suboptimal environmental conditions that result in seed ageing and high levels of genome damage. However, the mutagenic and...

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Autores principales: Waterworth, Wanda M., West, Christopher E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Portland Press Ltd. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10212508/
https://www.ncbi.nlm.nih.gov/pubmed/36947444
http://dx.doi.org/10.1042/BCJ20230006
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author Waterworth, Wanda M.
West, Christopher E.
author_facet Waterworth, Wanda M.
West, Christopher E.
author_sort Waterworth, Wanda M.
collection PubMed
description Successful germination and seedling establishment are important determinants of crop yields and plant survival in natural environments. Germination potential is compromised by suboptimal environmental conditions that result in seed ageing and high levels of genome damage. However, the mutagenic and growth inhibitory potential of DNA damage accumulated in seeds on subsequent seedling growth remains largely unknown. Arabidopsis seeds deficient in the chromosomal break repair factors DNA LIGASE 4 and DNA LIGASE 6 exhibited hypersensitivity to the effects of natural ageing, with reduced germination vigour and seedling biomass relative to wild type seed. Here, we identify that aged Arabidopsis seed display elevated levels of programmed cell death (PCD) in the root meristem which persists into seedling establishment, with higher levels of cell death in lines deficient in DNA double strand break repair. Reporter lines determined the effects of seed ageing on mutation levels and intrachromosomal recombination frequencies. Seed deterioration resulted in strikingly elevated levels of frameshift mutations and genome instability in germinated seedlings. Thus, elevated levels genome damage incurred in the seed stage of the plant life cycle potentially impacts significantly on subsequent plant development. Furthermore, the mutagenic effects of seed ageing has potentially long-term implications on the genome stability of plant populations and ecosystem fitness. Collectively, we identify genome damage accumulated in suboptimal quality seed impacts on subsequent plant growth and genome stability, with associated implications for crop yields and plant survival under changing climates.
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spelling pubmed-102125082023-05-26 Genome damage accumulated in seed ageing leads to plant genome instability and growth inhibition Waterworth, Wanda M. West, Christopher E. Biochem J Plant Biology Successful germination and seedling establishment are important determinants of crop yields and plant survival in natural environments. Germination potential is compromised by suboptimal environmental conditions that result in seed ageing and high levels of genome damage. However, the mutagenic and growth inhibitory potential of DNA damage accumulated in seeds on subsequent seedling growth remains largely unknown. Arabidopsis seeds deficient in the chromosomal break repair factors DNA LIGASE 4 and DNA LIGASE 6 exhibited hypersensitivity to the effects of natural ageing, with reduced germination vigour and seedling biomass relative to wild type seed. Here, we identify that aged Arabidopsis seed display elevated levels of programmed cell death (PCD) in the root meristem which persists into seedling establishment, with higher levels of cell death in lines deficient in DNA double strand break repair. Reporter lines determined the effects of seed ageing on mutation levels and intrachromosomal recombination frequencies. Seed deterioration resulted in strikingly elevated levels of frameshift mutations and genome instability in germinated seedlings. Thus, elevated levels genome damage incurred in the seed stage of the plant life cycle potentially impacts significantly on subsequent plant development. Furthermore, the mutagenic effects of seed ageing has potentially long-term implications on the genome stability of plant populations and ecosystem fitness. Collectively, we identify genome damage accumulated in suboptimal quality seed impacts on subsequent plant growth and genome stability, with associated implications for crop yields and plant survival under changing climates. Portland Press Ltd. 2023-04-04 /pmc/articles/PMC10212508/ /pubmed/36947444 http://dx.doi.org/10.1042/BCJ20230006 Text en © 2023 The Author(s) https://creativecommons.org/licenses/by/4.0/This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) . Open access for this article was enabled by the participation of University of Leeds in an all-inclusive Read & Publish agreement with Portland Press and the Biochemical Society under a transformative agreement with JISC.
spellingShingle Plant Biology
Waterworth, Wanda M.
West, Christopher E.
Genome damage accumulated in seed ageing leads to plant genome instability and growth inhibition
title Genome damage accumulated in seed ageing leads to plant genome instability and growth inhibition
title_full Genome damage accumulated in seed ageing leads to plant genome instability and growth inhibition
title_fullStr Genome damage accumulated in seed ageing leads to plant genome instability and growth inhibition
title_full_unstemmed Genome damage accumulated in seed ageing leads to plant genome instability and growth inhibition
title_short Genome damage accumulated in seed ageing leads to plant genome instability and growth inhibition
title_sort genome damage accumulated in seed ageing leads to plant genome instability and growth inhibition
topic Plant Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10212508/
https://www.ncbi.nlm.nih.gov/pubmed/36947444
http://dx.doi.org/10.1042/BCJ20230006
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