Transgenerational Adaptation of Arabidopsis to Stress Requires DNA Methylation and the Function of Dicer-Like Proteins

Abstract

Epigenetic states and certain environmental responses in mammals and seed plants can persist in the next sexual generation. These transgenerational effects have potential adaptative significance as well as medical and agronomic ramifications. Recent evidence suggests that some abiotic and biotic stress responses of plants are transgenerational. For example, viral infection of tobacco plants and exposure of Arabidopsis thaliana plants to UVC and flagellin can induce transgenerational increases in homologous recombination frequency (HRF). Here we show that exposure of Arabidopsis plants to stresses, including salt, UVC, cold, heat and flood, resulted in a higher HRF, increased global genome methylation, and higher tolerance to stress in the untreated progeny. This transgenerational effect did not, however, persist in successive generations. Treatment of the progeny of stressed plants with 5-azacytidine was shown to decrease global genomic methylation and enhance stress tolerance. Dicer-like (DCL) 2 and DCL3 encode Dicer activities important for small RNA-dependent gene silencing. Stress-induced HRF and DNA methylation were impaired in dcl2 and dcl3 deficiency mutants, while in dcl2 mutants, only stress-induced stress tolerance was impaired. Our results are consistent with the hypothesis that stress-induced transgenerational responses in Arabidopsis depend on altered DNA methylation and smRNA silencing pathways.

Life at the extreme: lessons from the genome

“…The concept of trans-generational epigenetic stress signatures has support from some studies. For example, when Arabidopsis parent populations were exposed to abiotic stresses that increased global methylation, their progeny were more stress tolerant [63]. Similarly, in rice, parents with hypermethylation of particular loci in response to low-nutrient stress produced progeny with increased tolerance [64].…”

Changes in homologous recombination frequency in Arabidopsis thaliana plants exposed to stress depend on time of exposure during development and on duration of stress exposure

“…Various stresses were shown to alter HRF in the progeny, including exposures to UV-C, temperature changes, salt and paraquat as well as infection with pathogens (Boyko et al 2010a;Kathiria et al 2010;Molinier et al 2006;Pecinka et al 2009). The majority of these stresses were applied to plants at a young age (7 dpg), although several of them were applied at 12 dpg or later (Pecinka et al 2009).…”

“…Abiotic and biotic stresses are known to destabilize the plant genome, although only a few of them, such as UV-C, ionizing radiation and certain chemicals, damage DNA directly (Boyko et al 2010b;Kovalchuk et al 2000). The great majority of stresses, such as water availability, salt, temperature fluctuations or infection with pathogens, are not known to damage DNA directly, but they may do so through free radicals, signaling, changes in DNA methylation and chromatin structure and the efficiency of DNA repair (Boyko et al 2010a;Roldan-Arjona and Ariza 2009;Zhang et al 2009). …”

“…Many stresses were shown to alter the frequency of somatic homologous recombination (HRF), including gamma-and Xrays, exposures to UV-C and UV-B, treatments with chemicals causing oxidative stress, herbicides as well as changes in temperature and water regimes and infection with pathogens (Besplug et al 2004;Boyko et al 2005Boyko et al , 2010aFilkowski et al 2004;Kathiria et al 2010;Kovalchuk et al 2000;Lucht et al 2002;Molinier et al 2005;Pecinka et al 2009;Ries et al 2000;Yao and Kovalchuk 2011). The influence of stress on the frequency of homologous recombination cannot be underestimated since HR is able to rearrange the plant genome substantially, thus leading to loss of heterozygocity.…”

“…Exposure to stress is also known to influence the frequency of meiotic recombination (Kovalchuk et al 2003;Ries et al 2000). Moreover, several experiments showed that the progeny of stressed plants exhibited higher levels of somatic HRF without being exposed to any stress (Boyko et al 2007(Boyko et al , 2010a; Kathiria et al 2010;Molinier et al 2006;Pecinka et al 2009).…”