Multigenerational Exposure to Heat Stress Induces Phenotypic Resilience, and Genetic and Epigenetic Variations in Arabidopsis thaliana Offspring

Yadav, Narendra Singh; Titov, Viktor; Ayemere, Ivie; Byeon, Boseon; Ilnytskyy, Yaroslav; Kovalchuk, Igor

doi:10.3389/fpls.2022.728167

Cited by 21 publications

(17 citation statements)

References 102 publications

(168 reference statements)

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“…Are the stochastic and deterministic route therefore two extremes of the same process? One argument holds against this: in A. thaliana , spontaneous epimutations mostly accumulate in the CG context (Becker et al, 2011; Denkena et al, 2021; Schmitz et al, 2011; van der Graaf et al, 2015) whereas environment-induced epialleles are most prominent in the CHG and/or CHH context (Annacondia et al, 2021; Lin et al, 2022; Wibowo et al, 2016; Yadav et al, 2022; Zhou et al, 2019). This supports the idea that the stochastic and deterministic route are, at least in the context of DNA methylation in plants, two fundamentally different processes.…”

Section: Discussionmentioning

confidence: 99%

Assessing rapid adaptation through epigenetic inheritance: a new experimental approach

Chávez,

Huber

2023

Preprint

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1. Epigenetic inheritance is hypothesized to mediate rapid adaptation to stresses via two fundamentally different routes: first, through spontaneous epimutations that arise in a largely stochastic manner in the presence or absence of stress; if these spontaneous epimutations are heritable and beneficial, they may be selected upon ('stochastic route'); and second, through environment-induced epialleles that arise uniformly among individuals; if heritable, these epialleles may lead to stress adaptation even in the absence of selection ('deterministic route'). Testing and teasing apart these two routes is challenging, largely because a suitable experimental approach is lacking. 2. Here, we propose an experimental approach that allows to simultaneously assess the contribution of the stochastic and deterministic route. The essence of the approach is to manipulate the efficacy of selection through the population size and thereby to test whether selection is required for adaptation (stochastic route). To this end, genetically uniform populations are grown under different environments across multiple generations ('pre-treatment') at two different population sizes: in large populations, in which selection is effective; and in small populations, in which drift overcomes the effect of selection. If the deterministic route contributes to adaptation, variation in fitness, phenotypes or epigenetic marks will arise between the small populations of the different pre-treatments. If the stochastic route contributes to adaptation, variation will arise between the small and large population within each pre-treatment. As a proof-of-principle, we tested whether small and large monoclonal populations of the aquatic duckweed Spirodela polyrhiza may adapt to copper excess outdoors. 3. After five to seven generations of pre-treatment and a subsequent multi-generational growth under control conditions, large populations outperformed small populations under copper excess. Furthermore, small populations pre-treated with copper excess tended to have higher fitness under copper excess than small populations pre-treated under control conditions. These data suggest that both the stochastic and deterministic route may alter plant fitness under recurring stress. 4. The proposed approach will allow to experimentally evaluate whether species may adapt to stresses through either stochastic and deterministic epigenetic changes, which is fundamental to understand whether and how epigenetic inheritance may lead to rapid stress adaptation.

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Section: Discussionmentioning

confidence: 99%

Assessing rapid adaptation through epigenetic inheritance: a new experimental approach

Chávez,

Huber

2023

Preprint

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“…Most of the environmentally induced memories are relatively short and can exist only as somatic memories. Occasionally, somatic stress memory persists to the next generation, resulting in changes in genome stability, plant morphology and stress tolerance [ 4 , 5 , 6 , 7 ]. This process is known as intergenerational stress response.…”

Section: Introductionmentioning

confidence: 99%

“…This process is known as intergenerational stress response. And even less frequently, the memory of stress exposure is carried yet to another generation, without stress exposure, resulting in so called transgenerational stress response [ 7 , 8 ]. It has been well documented that a transgenerational memory can play a role in generating epigenetic variants, in the form of differential DNA methylation or/and histone modifications that can allow plants to exhibit a certain degree of tolerance to the environmental stresses and consequently lead to adaptation [ 2 , 9 ].…”

Section: Introductionmentioning

confidence: 99%

“…Arabidopsis plants exposed to cold stress exhibit changes in the transposon expression and recombination frequency [ 12 ]. In response to heat stress, changes in the phenotypes, genotypes and epigenotypes have already been reported in Arabidopsis thaliana [ 7 , 13 ]. Several studies in Arabidopsis thaliana suggest that environmental stresses may also lead to an increase in the genomic diversity in the plants’ progeny, even in the untreated generations, and they potentially result in the adaptation to adverse conditions [ 7 , 14 , 15 , 16 , 17 ].…”

Section: Introductionmentioning

confidence: 99%

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Genomic and Epigenomic Changes in the Progeny of Cold-Stressed Arabidopsis thaliana Plants

Rahman,

Yadav,

Byeon

et al. 2024

IJMS

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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 Arabidopsis thaliana 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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“…Many studies have shown that transgenerational effects can influence offspring performance in many sexually propagated plants (Wang, 2005; Yadav et al, 2022; Zhang et al, 2013). However, the transgenerational effects may be more significant in asexually propagated plants (i.e., clonal plants) because they reproduce mainly via vegetative growth, so their offspring are more likely to encounter the same environment conditions as their parents (Hung et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Transgenerational competition effects persist across multiple generations and are altered by offspring competitive environments in a clonal plant

Jin

Chen

Lei

et al. 2023

Plant Species Biology

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Environments experienced by parental plants may potentially influence the performance of their offspring. These effects may also vary depending on the current environment experienced by the offspring. However, whether these transgenerational effects, especially those induced by biotic factors such as competition, can persist for multiple generations has not been tested. Here, we examined intraspecific competition‐induced transgenerational effects across multiple generations using a floating clonal plant Spirodela polyrhiza, by growing three successive generations each under either low or high density. The second‐generation offspring performed better when the first‐generation plants were grown under low than under high density, independently of the density experienced by the second generation. The third‐generation offspring performed better under low than under high density, and the difference was more pronounced when the second‐generation plants were grown under low density. Moreover, the density of the first and second generation interacted to influence the morphology of the third‐generation offspring. These results indicate that competition‐induced transgenerational effects in S. polyrhiza can vary depending on the competition environment of its offspring and that these effects can persist across multiple generations.

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Multigenerational Exposure to Heat Stress Induces Phenotypic Resilience, and Genetic and Epigenetic Variations in Arabidopsis thaliana Offspring

Cited by 21 publications

References 102 publications

Assessing rapid adaptation through epigenetic inheritance: a new experimental approach

Assessing rapid adaptation through epigenetic inheritance: a new experimental approach

Genomic and Epigenomic Changes in the Progeny of Cold-Stressed Arabidopsis thaliana Plants

Transgenerational competition effects persist across multiple generations and are altered by offspring competitive environments in a clonal plant

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