Low relative humidity triggers RNA-directed de novo DNA methylation and suppression of genes controlling stomatal development

Abstract

Environmental cues influence the development of stomata on the leaf epidermis, and allow plants to exert plasticity in leaf stomatal abundance in response to the prevailing growing conditions. It is reported that Arabidopsis thaliana ‘Landsberg erecta’ plants grown under low relative humidity have a reduced stomatal index and that two genes in the stomatal development pathway, SPEECHLESS and FAMA, become de novo cytosine methylated and transcriptionally repressed. These environmentally-induced epigenetic responses were abolished in mutants lacking the capacity for de novo DNA methylation, for the maintenance of CG methylation, and in mutants for the production of short-interfering non-coding RNAs (siRNAs) in the RNA-directed DNA methylation pathway. Induction of methylation was quantitatively related to the induction of local siRNAs under low relative humidity. Our results indicate the involvement of both transcriptional and post-transcriptional gene suppression at these loci in response to environmental stress. Thus, in a physiologically important pathway, a targeted epigenetic response to a specific environmental stress is reported and several of its molecular, mechanistic components are described, providing a tractable platform for future epigenetics experiments. Our findings suggest epigenetic regulation of stomatal development that allows for anatomical and phenotypic plasticity, and may help to explain at least some of the plant’s resilience to fluctuating relative humidity.

The Arabidopsis DNA Methylome Is Stable under Transgenerational Drought Stress

“…6, A and B). Interestingly, both loci were found to be largely devoid of DNA methylation across all experimental samples, comparable to the unmethylated nonstressed plants reported previously (Tricker et al, 2012). However, there was no evidence of any transmissible hypermethylation at these loci, neither lineage dependent nor drought dependent.…”

“…One of the key responses to drought stress is stomatal closure (Verslues et al, 2006), and recent investigations have found that environmentally induced variation in stomatal development and index is regulated, at least in part, by DNA methylation, with some evidence for DNA methylation-mediated transgenerational transmission (Tricker et al, 2012(Tricker et al, , 2013. Greater stomatal control to prevent dehydration would be beneficial under water limitation; therefore, stomatal responsiveness was compared between lineages.…”

“…Low humidity-induced hypermethylation at the FAMA and SPCH loci was described to be transmitted to progeny in Landsberg erecta (Tricker et al, 2012(Tricker et al, , 2013. These loci were profiled across P 1 progeny of G 0 and G 5 plants to look for evidence of hypermethylation (Fig.…”

Stomatal Development in Arabidopsis

“…Farquhar, 2001). The regulation of stomatal movement is coordinately controlled by a large network of signaling pathways that monitor water status, light, CO 2 and various other environmental conditions to optimize plant growth and water use (Schroeder et al, 2001;Shimazaki et al, 2007;Casson and Hetherington, 2010;Tricker et al, 2012). Numerous Arabidopsis mutants have been isolated that are defective in stomatal function (Gray et al, 2000;Assmann, 2003;Miyazawa et al, 2006;Young et al, 2006;Kang et al, 2009a;Clark et al, 2011;Sawinski et al, 2013).…”

Genome-Wide Characterization of Maize Small RNA Loci and Their Regulation in the required to maintain repression6-1 (rmr6-1) Mutant and Long-Term Abiotic Stresses

“…RdDM is also required for basal heat tolerance in Arabidopsis (Popova et al, 2013). Environmental stresses trigger the expression of siRNAs that modulate target genes involved in the stress response (Tricker et al, 2012;Wang et al, 2015). RdDM-associated siRNAs can also defend the genome from heat-induced movements of TEs (Ito et al, 2011).…”