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. 2010 May;3(3):594-602.
doi: 10.1093/mp/ssq014. Epub 2010 Apr 21.

Transgenerational Inheritance and Resetting of Stress-Induced Loss of Epigenetic Gene Silencing in Arabidopsis

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Free PMC article

Transgenerational Inheritance and Resetting of Stress-Induced Loss of Epigenetic Gene Silencing in Arabidopsis

Christina Lang-Mladek et al. Mol Plant. .
Free PMC article

Abstract

Plants, as sessile organisms, need to sense and adapt to heterogeneous environments and have developed sophisticated responses by changing their cellular physiology, gene regulation, and genome stability. Recent work demonstrated heritable stress effects on the control of genome stability in plants--a phenomenon that was suggested to be of epigenetic nature. Here, we show that temperature and UV-B stress cause immediate and heritable changes in the epigenetic control of a silent reporter gene in Arabidopsis. This stress-mediated release of gene silencing correlated with pronounced alterations in histone occupancy and in histone H3 acetylation but did not involve adjustments in DNA methylation. We observed transmission of stress effects on reporter gene silencing to non-stressed progeny, but this effect was restricted to areas consisting of a small number of cells and limited to a few non-stressed progeny generations. Furthermore, stress-induced release of gene silencing was antagonized and reset during seed aging. The transient nature of this phenomenon highlights the ability of plants to restrict stress-induced relaxation of epigenetic control mechanisms, which likely contributes to safeguarding genome integrity.

Figures

Figure 1.
Figure 1.
Phenotypes and TS–GUS Activity of Transgenic Arabidopsis thaliana Plants Immediately and 1 Week after UV-B (A), Heat (B), and Freezing (C) Stress. Blue areas indicate alleviation of TS–GUS silencing, which is very pronounced in response to heat and UV-B stress ctr.: non-stressed individuals in the same developmental stage. Arrow indicates GUS-positive organs that developed after stress application. Bar = 2 mm.
Figure 2.
Figure 2.
Expression of TS–GUS and Silenced Transposable Elements in Response to Abiotic Stress. (A) qRT–PCR performed on TS–GUS plants in the stressed S0 generation and in non-stressed S1 progeny. Transcript levels of TS–GUS and of a non-LTR retrotransposon (LINE039) show a significant increase in the S0 but not in the S1 generation. Expression levels were normalized to non-stressed controls (ctr). Standard deviations are indicated as bars. Similarly, transcript levels of TSI (B) and of additional non-LTR retrotransposons ((C); LINE018, LINE118, LINE315) show a significant increase in the S0 but not in the S1 generation.
Figure 3.
Figure 3.
Analysis of DNA Methylation and of the Chromatin Status at the TS–GUS Locus. (A) Graphic representation of the DNA methylation of TS–GUS in response to UV-B and temperature stress. Ordinates correspond to percent methylation in the entire set of samples analyzed by bisulfite sequencing (n = 20). Differences between samples derived from control (top) and stressed (bottom) plants are indicated as bars (middle). Nucleotide positions are indicated at the x-axes. (B) Chromatin immunoprecipitation performed with chromatin derived from UV-B, heat-stressed, and non-stressed control plants. Top left: histone H3 occupancy at the TS–GUS locus under ambient (control) and stressed conditions. Shown are values after normalization to the corresponding input fraction. Top right; bottom: histone H3 modifications at the TS–GUS locus under ambient (control) and stressed conditions. Values are normalized to control IPs performed with non-discriminating antibodies against histone H3. Standard deviations are indicated as bars. (C) Comparison of TS–GUS activity in 14-day-old wild-type (WT, left) and rts1-1 (right) plantlets.
Figure 4.
Figure 4.
Heritability and Resetting of Stress Effects on TS–GUS Activity. (A) TS–GUS activity (arrows) on rosette leaves of non-stressed progeny (G1, left; S1, right) derived from UV-B stressed (S0) and non-stressed (G0) parental plants. Bar = 0.5 mm. (B) TS–GUS reactivation in F1 plants of reciprocal crosses, for which one parent has been exposed to UV-B stress. Asterisks indicate a significant difference (p < 0.05) between the progeny of these crosses and the F1 progeny derived from crosses performed with non-stressed parents (= 100%). (C) Quantitative comparison of TS–GUS reactivation in the progeny of stressed plants (S1–S3). All values are normalized to GUS-positive areas of same-generation, non-stressed controls grown and scored in parallel (six). UV-B and freezing stress caused a significant increase in GUS reactivation in the S1 and S2 progeny, which was no longer detectable in the S3 generation. In heat-stressed plants, a significant increase in TS–GUS reactivation was observed in the S2 generation, which was no longer detected in the S3 generation. Asterisks indicate a significant difference (p < 0.05) between the progeny of stressed plants and their respective non-stressed controls (= 100%). (D, E) Seed age correlates with resetting of TS–GUS reactivation in the S1 (D) and the S2 (E) generation. Asterisks indicate a significant difference (p < 0.05) when comparing TS–GUS activity in seedlings scored immediately after seed harvesting with TS–GUS activity in seedlings after seed storage for the time periods indicated. All values are normalized to GUS-positive areas of non-stressed controls (G1 and G2) grown in parallel (= 100%).

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