PHYTOCHROME B and HISTONE DEACETYLASE 6 Control Light-Induced Chromatin Compaction in Arabidopsis thaliana

Abstract

Natural genetic variation in Arabidopsis thaliana exists for many traits and often reflects acclimation to local environments. Studying natural variation has proven valuable in the characterization of phenotypic traits and, in particular, in identifying genetic factors controlling these traits. It has been previously shown that chromatin compaction changes during development and biotic stress. To gain more insight into the genetic control of chromatin compaction, we investigated the nuclear phenotype of 21 selected Arabidopsis accessions from different geographic origins and habitats. We show natural variation in chromatin compaction and demonstrate a positive correlation with latitude of geographic origin. The level of compaction appeared to be dependent on light intensity. A novel approach, combining Quantitative Trait Locus (QTL) mapping and microscopic examination, pointed at PHYTOCHROME-B (PHYB) and HISTONE DEACETYLASE-6 (HDA6) as positive regulators of light-controlled chromatin compaction. Indeed, mutant analyses demonstrate that both factors affect global chromatin organization. HDA6, in addition, strongly promotes the light-mediated compaction of the Nucleolar Organizing Regions (NORs). The accession Cape Verde Islands-0 (Cvi-0), which shows sequence polymorphism in the PHYB gene and in the HDA6 promotor, resembles the hda6 mutant in having reduced chromatin compaction and decreased methylation levels of DNA and histone H3K9 at the NORs. We provide evidence that chromatin organization is controlled by light intensity. We propose that chromatin plasticity is associated with acclimation of Arabidopsis to its environment. The polymorphic alleles such as PHYB and HDA6 control this process.

Epigenetic Regulation of Repetitive Elements Is Attenuated by Prolonged Heat Stress in Arabidopsis

“…Since this was specific for ecotypes that originate from low geographical latitudes with naturally high light intensity, this can also be seen as a stress response. While life-long culture of these plants at higher light intensity could eliminate the phenotype of CC decondensation (Tessadori et al, 2009), the study does not address whether already decondensed chromatin could revert to the regular configuration by a switch in light conditions, which is a question of interest in the context of our data. Nevertheless, decondensation of heterochromatin is not a general response to stress, since we did not observe this phenotype after freezing (248C for 24 h) or UV-C irradiation (3000 J/m 2 ).…”

“…Heterochromatin decondensation per se was not sufficient for repeat activation (Tessadori et al, 2007b). More permanent and even repeat-specific heterochromatin decondensation has been described for plants grown at low light intensity (Tessadori et al, 2009). Since this was specific for ecotypes that originate from low geographical latitudes with naturally high light intensity, this can also be seen as a stress response.…”

Chromosome Organization and Dynamics during Interphase, Mitosis, and Meiosis in Plants

“…Both processes are affected by light conditions. Furthermore, Arabidopsis genotypes acclimated to different latitudes exhibit genetically programmed levels of chromatin compaction, depending on the light intensity of their original habitats (Tessadori et al, 2009). In rice, heat stress has been shown to induce chromatin decondensation (Santos et al, 2011).…”

Evolutionary Studies Illuminate the Structural-Functional Model of Plant Phytochromes

“…Natural populations of most species harbor extensive variation, and particularly where genomic and genetic resources are also available, they offer a useful set of genetic polymorphisms for study (e.g., AlonsoBlanco and Koornneef, 2000;Shindo et al, 2005;Buckler et al, 2009;McMullen et al, 2009). Studies of natural variation have been used to map quantitative trait loci controlling responses to light, dark, and cold in Arabidopsis Borevitz et al, 2002;Meng et al, 2008), to identify accessions that vary in responses to R or FR light (Maloof et al, 2001;Botto and Smith, 2002;Filiault et al, 2008) or in phytochrome activities (Eichenberg et al, 2000b), to infer a role for phyB in chromatin compaction (Tessadori et al, 2009), and to investigate the basis of plastic responses to shifts in the R:FR ratio (Brock et al, 2007). Natural variation in phytochrome responses has been detected in other species, including barley (Hordeum vulgare; Biyashev et al, 1997), oat (Avena sativa; Hou and Simpson, 1993), and Plantago lanceolata (Van Hinsberg, 1998), and single nucleotide polymorphisms at PHYB are candidates for causal linkage with clinal variation in bud set in Populus tremula (Ingvarsson et al, 2006).…”