Transgenerational response to stress in<i>Arabidopsis thaliana</i>

Boyko, Alex; Kovalchuk, Igor

doi:10.4161/psb.5.8.12227

Cited by 73 publications

(55 citation statements)

References 23 publications

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“…Often, changes in response to stress such as temperature are reversible, but in certain cases these modifications, including phenotypic and epigenetic, may be passed on to the progeny. 8,9 Epigenetic systems have the dynamic ability to rapidly induce changes in response to stress, resulting in modifications that may be short or long-term. [10][11][12] For example, environmental stress has been shown to cause hypo-or hypermethylation, altering the accessibility of chromatin to recombination machinery, and thus modifying variability in the genome at a time when it is most needed.…”

Section: Introductionmentioning

confidence: 99%

Transgenerational phenotypic and epigenetic changes in response to heat stress inArabidopsis thaliana

Migicovsky

Yao

Kovalchuk

2014

Plant Signaling & Behavior

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Abbreviations: ChiP, chromatin immunoprecipitation; DCL, Dicer-like; Dpg, days post germination; gDNA, genomic DNA; "C 1 ," progeny of control plants; "C 1 -", progeny of control plants grown under normal conditions; "C 1 +," progeny of control plants grown under stress conditions; "S 1 ," progeny of stress plants; "S 1 -," progeny of stressed plants grown under normal conditions; "S 1 +," progeny of stressed plants grown under stress conditions; qPCR, quantitative PCR; RdDM, RNA-directed DNA methylation; SAR, systemic acquired resistance; sRNAs, small RNAs; TE, transposable elements exposure to heat stress causes physiological and epigenetic changes in plants, which may also be altered in the progeny. We compared the progeny of stressed and control Arabidopsis thaliana wild type and Dicer-like mutant dcl2, dcl3, and dcl4 plants for variations in physiology and molecular profile, including global genome methylation, mRNa levels, and histone modifications in the subset of differentially expressed genes at normal conditions and in response to heat stress. We found that the immediate progeny of heat-stressed plants had fewer, but larger leaves, and tended to bolt earlier. Transposon expression was elevated in the progeny of heat-stressed plants, and heat stress in the same generation tended to decrease global genome methylation. Progeny of stressed plants had increased expression of HSFA2, and reduction in MSH2, ROS1, and several SUVH genes. Gene expression positively correlated with permissive histone marks and negatively correlated with repressive marks. Overall, the progeny of heat stressed plants varied in both their physiology and epigenome and dcl2 and dcl3 mutants were partially deficient for these changes.

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Section: Introductionmentioning

confidence: 99%

Transgenerational phenotypic and epigenetic changes in response to heat stress inArabidopsis thaliana

Migicovsky

Yao

Kovalchuk

2014

Plant Signaling & Behavior

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“…Previous work has revealed that DNA polymerase activity decreases in older plants (Bottomley, 1970;Golubov et al, 2010), and if this age-related down-regulation is epigenetically transmitted to the progeny, it may affect somatic mutation rates. Such a down-regulation of gene expression may result from the inheritance of DNA methylation patterns, histone modifications, or small RNAs that mediate gene silencing (Brennecke et al, 2008;Boyko and Kovalchuk, 2010).…”

Section: Saal 2000)mentioning

confidence: 99%

Parental Age Affects Somatic Mutation Rates in the Progeny of Flowering Plants

et al. 2015

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In humans, it is well known that the parental reproductive age has a strong influence on mutations transmitted to their progeny. Meiotic nondisjunction is known to increase in older mothers, and base substitutions tend to go up with paternal reproductive age. Hence, it is clear that the germinal mutation rates are a function of both maternal and paternal ages in humans. In contrast, it is unknown whether the parental reproductive age has an effect on somatic mutation rates in the progeny, because these are rare and difficult to detect. To address this question, we took advantage of the plant model system Arabidopsis (Arabidopsis thaliana), where mutation detector lines allow for an easy quantitation of somatic mutations, to test the effect of parental age on somatic mutation rates in the progeny. Although we found no significant effect of parental age on base substitutions, we found that frameshift mutations and transposition events increased in the progeny of older parents, an effect that is stronger through the maternal line. In contrast, intrachromosomal recombination events in the progeny decrease with the age of the parents in a parent-of-origin-dependent manner. Our results clearly show that parental reproductive age affects somatic mutation rates in the progeny and, thus, that some form of age-dependent information, which affects the frequency of double-strand breaks and possibly other processes involved in maintaining genome integrity, is transmitted through the gametes.

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“…Because homologous recombination is involved in the repair of single and double DNA strand breaks as well as the generation of gene duplications, translocations, and gross chromosomal rearrangements (Puchta, 2005), the level of HRF is an overall indicator of the level of genome rearrangement, which in turn is an indicator of genomic instability. Using an HRF reporter, we previously demonstrated an increase in HRF in response to various environmental stresses, including UV-C (Filkowski et al, 2004;Boyko et al, 2006aBoyko et al, , 2006bBoyko et al, , 2010aBoyko et al, , 2010bBoyko and Kovalchuk, 2010). We showed that systemic changes in HRF, referred to as the systemic recombination signal, were generated in stressed tissues, transported to naive nonstressed tissues, and inherited in subsequent generations (Kovalchuk et al, 2003;Boyko et al, 2007;.…”

Section: Introductionmentioning

confidence: 99%

UV-C–Irradiated Arabidopsis and Tobacco Emit Volatiles That Trigger Genomic Instability in Neighboring Plants

et al. 2011

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We have previously shown that local exposure of plants to stress results in a systemic increase in genome instability. Here, we show that UV-C–irradiated plants produce a volatile signal that triggers an increase in genome instability in neighboring nonirradiated Arabidopsis thaliana plants. This volatile signal is interspecific, as UV-C–irradiated Arabidopsis plants transmit genome destabilization to naive tobacco (Nicotiana tabacum) plants and vice versa. We report that plants exposed to the volatile hormones methyl salicylate (MeSA) or methyl jasmonate (MeJA) exhibit a similar level of genome destabilization as UV-C–irradiated plants. We also found that irradiated Arabidopsis plants produce MeSA and MeJA. The analysis of mutants impaired in the synthesis and/or response to salicylic acid (SA) and/or jasmonic acid showed that at least one other volatile compound besides MeSA and MeJA can communicate interplant genome instability. The NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 (npr1) mutant, defective in SA signaling, is impaired in both the production and the perception of the volatile signals, demonstrating a key role for NPR1 as a central regulator of genome stability. Finally, various forms of stress resulting in the formation of necrotic lesions also generate a volatile signal that leads to genomic instability.

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Transgenerational response to stress inArabidopsis thaliana

Cited by 73 publications

References 23 publications

Transgenerational phenotypic and epigenetic changes in response to heat stress inArabidopsis thaliana

Transgenerational phenotypic and epigenetic changes in response to heat stress inArabidopsis thaliana

Parental Age Affects Somatic Mutation Rates in the Progeny of Flowering Plants

UV-C–Irradiated Arabidopsis and Tobacco Emit Volatiles That Trigger Genomic Instability in Neighboring Plants

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