Genomic and Epigenomic Changes in the Progeny of Cold-Stressed <i>Arabidopsis thaliana</i> Plants

Plants are continuously exposed to various environmental stresses. Because they can not escape stress, they have to develop mechanisms of remembering stress exposures somatically and passing it to the progeny. We studied the <i>Arabidopsis thaliana</i> ecotype Columbia plants exposed to...

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Main Authors: Ashif Rahman, Narendra Singh Yadav, Boseon Byeon, Yaroslav Ilnytskyy, Igor Kovalchuk
Format: Article
Language:English
Published: MDPI AG 2024-02-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/25/5/2795
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author Ashif Rahman
Narendra Singh Yadav
Boseon Byeon
Yaroslav Ilnytskyy
Igor Kovalchuk
author_facet Ashif Rahman
Narendra Singh Yadav
Boseon Byeon
Yaroslav Ilnytskyy
Igor Kovalchuk
author_sort Ashif Rahman
collection DOAJ
description Plants are continuously exposed to various environmental stresses. Because they can not escape stress, they have to develop mechanisms of remembering stress exposures somatically and passing it to the progeny. We studied the <i>Arabidopsis thaliana</i> ecotype Columbia plants exposed to cold stress for 25 continuous generations. Our study revealed that multigenerational exposure to cold stress resulted in the changes in the genome and epigenome (DNA methylation) across generations. Main changes in the progeny were due to the high frequency of genetic mutations rather than epigenetic changes; the difference was primarily in single nucleotide substitutions and deletions. The progeny of cold-stressed plants exhibited the higher rate of missense non-synonymous mutations as compared to the progeny of control plants. At the same time, epigenetic changes were more common in the CHG (C = cytosine, H = cytosine, adenine or thymine, G = guanine) and CHH contexts and favored hypomethylation. There was an increase in the frequency of C to T (thymine) transitions at the CHH positions in the progeny of cold stressed plants; because this type of mutations is often due to the deamination of the methylated cytosines, it can be hypothesized that environment-induced changes in methylation contribute to mutagenesis and may be to microevolution processes and that RNA-dependent DNA methylation plays a crucial role. Our work supports the existence of heritable stress response in plants and demonstrates that genetic changes prevail.
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spelling doaj.art-5cbea36a4fa8499b9772ebe42b3a88222024-03-12T16:46:21ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672024-02-01255279510.3390/ijms25052795Genomic and Epigenomic Changes in the Progeny of Cold-Stressed <i>Arabidopsis thaliana</i> PlantsAshif Rahman0Narendra Singh Yadav1Boseon Byeon2Yaroslav Ilnytskyy3Igor Kovalchuk4Department of Biological Sciences, University of Lethbridge, Lethbridge, AB T1K 3M4, CanadaDepartment of Biological Sciences, University of Lethbridge, Lethbridge, AB T1K 3M4, CanadaBiomedical and Health Informatics, Computer Science Department, State University of New York, 2 S Clinton St, Syracuse, NY 13202, USADepartment of Biological Sciences, University of Lethbridge, Lethbridge, AB T1K 3M4, CanadaDepartment of Biological Sciences, University of Lethbridge, Lethbridge, AB T1K 3M4, CanadaPlants are continuously exposed to various environmental stresses. Because they can not escape stress, they have to develop mechanisms of remembering stress exposures somatically and passing it to the progeny. We studied the <i>Arabidopsis thaliana</i> ecotype Columbia plants exposed to cold stress for 25 continuous generations. Our study revealed that multigenerational exposure to cold stress resulted in the changes in the genome and epigenome (DNA methylation) across generations. Main changes in the progeny were due to the high frequency of genetic mutations rather than epigenetic changes; the difference was primarily in single nucleotide substitutions and deletions. The progeny of cold-stressed plants exhibited the higher rate of missense non-synonymous mutations as compared to the progeny of control plants. At the same time, epigenetic changes were more common in the CHG (C = cytosine, H = cytosine, adenine or thymine, G = guanine) and CHH contexts and favored hypomethylation. There was an increase in the frequency of C to T (thymine) transitions at the CHH positions in the progeny of cold stressed plants; because this type of mutations is often due to the deamination of the methylated cytosines, it can be hypothesized that environment-induced changes in methylation contribute to mutagenesis and may be to microevolution processes and that RNA-dependent DNA methylation plays a crucial role. Our work supports the existence of heritable stress response in plants and demonstrates that genetic changes prevail.https://www.mdpi.com/1422-0067/25/5/2795multigenerational cold stressstress memory<i>Arabidopsis thaliana</i>intergenerational inheritanceepigenetic variationsgenetic variations
spellingShingle Ashif Rahman
Narendra Singh Yadav
Boseon Byeon
Yaroslav Ilnytskyy
Igor Kovalchuk
Genomic and Epigenomic Changes in the Progeny of Cold-Stressed <i>Arabidopsis thaliana</i> Plants
International Journal of Molecular Sciences
multigenerational cold stress
stress memory
<i>Arabidopsis thaliana</i>
intergenerational inheritance
epigenetic variations
genetic variations
title Genomic and Epigenomic Changes in the Progeny of Cold-Stressed <i>Arabidopsis thaliana</i> Plants
title_full Genomic and Epigenomic Changes in the Progeny of Cold-Stressed <i>Arabidopsis thaliana</i> Plants
title_fullStr Genomic and Epigenomic Changes in the Progeny of Cold-Stressed <i>Arabidopsis thaliana</i> Plants
title_full_unstemmed Genomic and Epigenomic Changes in the Progeny of Cold-Stressed <i>Arabidopsis thaliana</i> Plants
title_short Genomic and Epigenomic Changes in the Progeny of Cold-Stressed <i>Arabidopsis thaliana</i> Plants
title_sort genomic and epigenomic changes in the progeny of cold stressed i arabidopsis thaliana i plants
topic multigenerational cold stress
stress memory
<i>Arabidopsis thaliana</i>
intergenerational inheritance
epigenetic variations
genetic variations
url https://www.mdpi.com/1422-0067/25/5/2795
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