(A.J.).Linker (H1) histones play critical roles in chromatin compaction in higher eukaryotes. They are also the most variable of the histones, with numerous nonallelic variants cooccurring in the same cell. Plants contain a distinct subclass of minor H1 variants that are induced by drought and abscisic acid and have been implicated in mediating adaptive responses to stress. However, how these variants facilitate adaptation remains poorly understood. Here, we show that the single Arabidopsis (Arabidopsis thaliana) stressinducible variant H1.3 occurs in plants in two separate and most likely autonomous pools: a constitutive guard cell-specific pool and a facultative environmentally controlled pool localized in other tissues. Physiological and transcriptomic analyses of h1.3 null mutants demonstrate that H1.3 is required for both proper stomatal functioning under normal growth conditions and adaptive developmental responses to combined light and water deficiency. Using fluorescence recovery after photobleaching analysis, we show that H1.3 has superfast chromatin dynamics, and in contrast to the main Arabidopsis H1 variants H1.1 and H1.2, it has no stable bound fraction. The results of global occupancy studies demonstrate that, while H1.3 has the same overall binding properties as the main H1 variants, including predominant heterochromatin localization, it differs from them in its preferences for chromatin regions with epigenetic signatures of active and repressed transcription. We also show that H1.3 is required for a substantial part of DNA methylation associated with environmental stress, suggesting that the likely mechanism underlying H1.3 function may be the facilitation of chromatin accessibility by direct competition with the main H1 variants.Linker (H1) histones are conserved and ubiquitous structural components of eukaryotic chromatin required for the stabilization of higher order chromatin structure and are generally thought to restrict DNA accessibility. Interestingly, despite their architectural role, H1 histones were shown to be highly mobile and continuously exchanging among chromatin-binding sites (Raghuram et al., 2009). They are also the most variable of the histones, with numerous nonallelic variants coexisting in the same cell. In vertebrates, several evolutionarily conserved subfamilies of H1 can be distinguished (Talbert et al., 2012) and appear to play both redundant and specific roles during development and cellular differentiation (McBryant et al., 2010). There is accumulating evidence that, in animals, regulation of the proportions of H1 variants with different dynamic behavior in chromatin is involved in controlling the accessibility of DNA to trans-acting factors (Jullien et al., 2010;Shahhoseini et al., 2010;Zhang et al., 2012a;Pérez-Montero et al., 2013;Christophorou et al., 2014).Epigenetic mechanisms, including DNA and histone modifications and active nucleosome remodeling, are major players in translating signals about environmental perturbations into adaptive responses at the transc...