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

Federico Tessadori,Rachel Clifton,Charles Spillane,Craig S Pikaard,Penka Pavlova,Laurentius A C J Voesenek,Martijn Van Zanten,Roel Van Driel,L Basten Snoek,Frédéric Pontvianne,Anton J M Peeters,Paul Fransz,Roeland Kees Schulkes,Frank F Millenaar,Gregory S Barsh

doi:10.1371/journal.pgen.1000638

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.

Highlights

Plant phenotypes are the integrated result of developmental programs and plastic responses to the environment
The habitat of the plant model species Arabidopsis thaliana can be found throughout the Northern hemisphere
We utilized this natural variation via a novel approach, combining microscopic examination, quantitative genetics, and analysis of environmental parameters, to understand the regulation of nuclear chromatin compaction in leaf mesophyll cells

Summary

Introduction

Plant phenotypes are the integrated result of developmental programs and plastic responses to the environment. Rich natural (genetic) variation exists among collected accessions [1,2,3,4], which are acclimated to environmental conditions in their local habitat. Utilization of this natural variation in functional studies has led to a better understanding of the molecular and physiological mechanisms of complex traits such as the acclimation to the light environment [5,6,7,8,9,10,11]. We recently observed variation in chromatin compaction during floral induction in three Arabidopsis accessions [12], suggesting the existence of natural genetic variation for chromatin organization. Quantification of chromocenter size and intensity has been used to assess chromatin compaction in several studies [12,14,15,16,17]

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Conclusion