Histone chaperones in Arabidopsis and rice: genome-wide identification, phylogeny, architecture and transcriptional regulation

Abstract

BackgroundHistone chaperones modulate chromatin architecture and hence play a pivotal role in epigenetic regulation of gene expression. In contrast to their animal and yeast counterparts, not much is known about plant histone chaperones. To gain insights into their functions in plants, we sought to identify histone chaperones from two model plant species and investigated their phylogeny, domain architecture and transcriptional profiles to establish correlation between their expression patterns and potential role in stress physiology and plant development.ResultsThrough comprehensive whole genome analyses of Arabidopsis and rice, we identified twenty-two and twenty-five genes encoding histone chaperones in these plants, respectively. These could be classified into seven different families, namely NAP, CAF1, SPT6, ASF1, HIRA, NASP, and FACT. Phylogenetic analyses of histone chaperones from diverse organisms including representative species from each of the major plant groups, yeast and human indicated functional divergence in NAP and CAF1C in plants. For the largest histone chaperone family, NAP, phylogenetic reconstruction suggested the presence of two distinct groups in plants, possibly with differing histone preferences. Further, to comment upon their physiological roles in plants, we analyzed their expression at different developmental stages, across various plant tissues, and under biotic and abiotic stress conditions using pre-existing microarray and qRT-PCR. We found tight transcriptional regulation of some histone chaperone genes during development in both Arabidopsis and rice, suggesting that they may play a role in genetic reprogramming associated with the developmental process. Besides, we found significant differential expression of a few histone chaperones under various biotic and abiotic stresses pointing towards their potential function in stress response.ConclusionsTaken together, our findings shed light onto the possible evolutionary trajectory of plant histone chaperones and present novel prospects about their physiological roles. Considering that the developmental process and stress response require altered expression of a large array of genes, our results suggest that some plant histone chaperones may serve a regulatory role by controlling the expression of genes associated with these vital processes, possibly via modulating chromatin dynamics at the corresponding genetic loci.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0414-8) contains supplementary material, which is available to authorized users.

A NAP-Family Histone Chaperone Functions in Abiotic Stress Response and Adaptation

“…However, there is a paucity of reports elucidating the role of plant histone chaperones in stress response and adaptation. Previously, through expression profiling of histone chaperones from rice and Arabidopsis, we had shown that a few putative histone chaperones show differential expression under various abiotic stress conditions (Tripathi et al, 2015). Out of the eight stress-regulated putative histone chaperones in rice, except the NAP family of proteins, all others are known to execute histone chaperone function as multimeric complexes formed by two or more polypeptides (De Koning et al, 2007;Tripathi et al, 2015); hence, altering the expression of a single member of such complexes might not show a phenotype.…”

“…The NAP family is generally considered to comprise H2A-H2B histone chaperones (De Koning et al, 2007). In our previous study, the phylogenetic analysis of NAP family proteins from yeast, humans, Arabidopsis (Arabidopsis thaliana), and rice showed that OsNAPL6 is evolutionarily closer to HsSET than to other NAP proteins from yeast and humans (Tripathi et al, 2015). HsSET, in spite of being a NAP family histone chaperone, is much different from other NAP family proteins showing binding preference toward the H3-H4 histones (Karetsou et al, 2009), while ScNAP1 and other NAP proteins from humans are considered to be H2A-H2B histone chaperones (De Koning et al, 2007;Park et al, 2005).…”

“…Because histone chaperones possess the capacity to modulate gene expression and DNA repair, they may potentially play a pivotal role in plant adaptation to various stresses, which remains to be studied in detail. Indicative findings of a few previous studies (Liu et al, 2009;Zhu et al, 2011Zhu et al, , 2013Weng et al, 2014;Tripathi et al, 2015) suggest that a few histone chaperones, such as ASF1 and NAP1;3, may function in abiotic stress response in plants. However, evidence showing their precise function while a plant responds and adapts to various abiotic stresses is lacking.…”

“…In a previous study (Tripathi et al, 2015), we identified 25 rice (Oryza sativa) genes encoding putative histone chaperones belonging to the seven major families viz. CAF1 (Chromatin assembly factor I), FACT (Facilitates chromatin transcription), ASF1 (Antisilencing factor 1), HIRA (Histone regulatory homolog A), NASP (Nuclear Autoantigenic Sperm Protein), SPT6 (Suppressor of Ty element 6), and NAP (Nucleosome Assembly Protein).…”

“…Via expression profiling, we found eight putative rice histone chaperones (two each from NAP and CAF1C and one each from CAF1A, CAF1B, SPT16, and SSRP families/subfamilies) to be responsive to multiple abiotic stress conditions. Apart from the members of the NAP family of proteins, all other abiotic stress-responsive rice histone chaperones are known to execute nucleosome assembly/disassembly function as multimeric complexes formed by two or more polypeptides (Eitoku et al, 2008;Tripathi et al, 2015).…”