AtFKBP53 is a histone chaperone required for repression of ribosomal RNA gene expression in Arabidopsis

Abstract

Chromatin structure is important for controlling gene expression, but mechanisms underlying chromatin remodeling are not fully understood. Here we report that an FKBP (FK506 binding protein) type immunophilin, AtFKBP53, possesses histone chaperone activity and is required for repressing ribosomal gene expression in Arabidopsis. The At-FKBP53 protein is a multidomain FKBP with a typical peptidylprolyl isomerase (PPIase) domain and several highly charged domains. Using nucleosome assembly assays, we showed that AtFKBP53 has histone chaperone activity and the charged acidic domains are sufficient for the activity. We show that AtFKBP53 interacts with histone H3 through the acidic domains, whereas the PPIase domain is dispensable for histone chaperone activity or histone binding. Ribosomal RNA gene (18S rDNA) is overexpressed when AtFKBP53 activity is reduced or eliminated in Arabidopsis plants. Chromatin immunoprecipitation assay showed that AtFKBP53 is associated with the 18S rDNA gene chromatin, implicating that AtFKBP53 represses rRNA genes at the chromatin level. This study identifies a new histone chaperone in plants that functions in chromatin remodeling and regulation of transcription.

The FKBP families of higher plants: Exploring the structures and functions of protein interaction specialists

“…AtFKBP53 localises to chromatin at 18S rRNA genes, indicating a role in histone deposition to regulate expression of the 18S ribosomal subunit. AtFKBP53 binds with histone via an N-terminal domain highly concentrated with acidic residues [56]. This domain is also seen in the duplicate AtFKBP43 [7] and in the rice paralogues OsFKBP53a and OsFKBP53b [8], indicating functional overlap between nuclear duplicates that may account for the lack of growth phenotypes in atfkbp53 and atfkbp43 gene knockouts [56].…”

“…Li and Luan [56] recently demonstrated a physical interaction between FKBP53 and the histone H3 subunit in Arabidopsis, implicated this nuclear FKBP in regulating gene expression. AtFKBP53 localises to chromatin at 18S rRNA genes, indicating a role in histone deposition to regulate expression of the 18S ribosomal subunit.…”

Genome wide analysis ofCyclophilingene family from rice and Arabidopsis and its comparison with yeast

“…The cellular role of the cyclophilins has been reported in signal transduction, 8,9 DNA transcription, 34 protein trafficking, 7 apoptosis 35 and fertility. 36 In plants, it is believed to play a potent role in abiotic stress tolerance, 37,38 hormone signaling, 39 chromatin remodelling process, 40 disease resistance. 41,42 Role of CYP20-3 (At3g62030) gene from Arabidopsis has been reported in light and other stress conditions.…”

Structure and Activity of the Peptidyl-Prolyl Isomerase Domain from the Histone Chaperone Fpr4 toward Histone H3 Proline Isomerization

“…However, this region may also serve a separate and distinct role in the full-length protein, because the N-terminal domain displays a isolated histone chaperone activity (11,12). This property of the N-terminal region has also been observed for the orthologous proteins FKBP39 from Schizosaccharomyces pombe (11) and FKBP53 from Arabidoposis thaliana (49).…”