Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome

Abstract

BackgroundIn arid and semi-arid environments, drought and soil salinity usually occur at the beginning and end of a plant's life cycle, offering a natural opportunity for the priming of young plants to enhance stress tolerance in mature plants. Chromatin marks, such as histone modifications, provide a potential molecular mechanism for priming plants to environmental stresses, but whether transient exposure of seedlings to hyperosmotic stress leads to chromatin changes that are maintained throughout vegetative growth remains unclear.ResultsWe have established an effective protocol for hyperosmotic priming in the model plant Arabidopsis, which includes a transient mild salt treatment of seedlings followed by an extensive period of growth in control conditions. Primed plants are identical to non-primed plants in growth and development, yet they display reduced salt uptake and enhanced drought tolerance after a second stress exposure. ChIP-seq analysis of four histone modifications revealed that the priming treatment altered the epigenomic landscape; the changes were small but they were specific for the treated tissue, varied in number and direction depending on the modification, and preferentially targeted transcription factors. Notably, priming leads to shortening and fractionation of H3K27me3 islands. This effect fades over time, but is still apparent after a ten day growth period in control conditions. Several genes with priming-induced differences in H3K27me3 showed altered transcriptional responsiveness to the second stress treatment.ConclusionExperience of transient hyperosmotic stress by young plants is stored in a long-term somatic memory comprising differences of chromatin status, transcriptional responsiveness and whole plant physiology.

Rapid hyperosmotic-induced Ca 2+ responses in Arabidopsis thaliana exhibit sensory potentiation and involvement of plastidial KEA transporters

“…However, the expression, activity, or sensitivity of the sensory components is increased after a previous experience of hyperosmotic stress, thereby exhibiting sensory potentiation. Important and interesting examples in the literature describe the enhancement of responses after experiencing stress, sometimes referred to as "priming" or "memory" (43)(44)(45)(46). The present study, however, reports that the earliest sensory components of the rapid osmotic stress response can be up-regulated in such a manner.…”

Osmotic stress induces phosphorylation of histone H3 at threonine 3 in pericentromeric regions of Arabidopsis thaliana

“…Changes in DNA methylation, several posttranslational histone modifications, as well as a linker histone H1 variant have been implicated in plant responses to osmotic/salt stress (2,3,6,10,20,21,(42)(43)(44)(45), but in most cases the relationship among chromatin status, transcriptional responsiveness, and physiological outcomes is not clearly understood. Interestingly, in both metazoans and plants, histone phosphorylation appears to be involved in responses to osmotic/salt stress (3,17,(19)(20)(21).…”

Histone Deacetylase Complex1 Expression Level Titrates Plant Growth and Abscisic Acid Sensitivity in Arabidopsis

“…Chromatin extraction and ChIP were performed using published protocols (Gendrel et al, 2002;Saleh et al, 2008;Sani et al, 2013). Tissue samples were incubated in 1% (w/v) formaldehyde for 15 min under vacuum.…”