The Arabidopsis Histone Chaperone FACT: Role of the HMG-Box Domain of SSRP1

Pfab, Alexander; Grønlund, Jesper T.; Holzinger, Philipp; Längst, Gernot; Grasser, Klaus D.

doi:10.1016/j.jmb.2018.06.046

Cited by 16 publications

(18 citation statements)

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“…In Arabidopsis, as the histone chaperone's subunit facilitates chromatin transcription (FACT) complex, SSRP1 has a role in maintaining cell identities and pollen fertility (Hossan et al, 2016;Frost et al, 2018;Kolundzic et al, 2018;Pfab et al, 2018). Our results further confirm that depletion of AtSSRP1 proteins has normal phenotypic mature pollen but leads to severe effects on the seed set (Figures 6A,B,F).…”

Section: Differential Histone Programs Between Vn and Gn Mediated By Specific Histone Chaperonessupporting

confidence: 78%

Proteomic Analysis of Generative and Vegetative Nuclei Reveals Molecular Characteristics of Pollen Cell Differentiation in Lily

et al. 2021

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In plants, the cell fates of a vegetative cell (VC) and generative cell (GC) are determined after the asymmetric division of the haploid microspore. The VC exits the cell cycle and grows a pollen tube, while the GC undergoes further mitosis to produce two sperm cells for double fertilization. However, our understanding of the mechanisms underlying their fate differentiation remains limited. One major advantage of the nuclear proteome analysis is that it is the only method currently able to uncover the systemic differences between VC and GC due to GC being engulfed within the cytoplasm of VC, limiting the use of transcriptome. Here, we obtained pure preparations of the vegetative cell nuclei (VNs) and generative cell nuclei (GNs) from germinating lily pollens. Utilizing these high-purity VNs and GNs, we compared the differential nucleoproteins between them using state-of-the-art quantitative proteomic techniques. We identified 720 different amount proteins (DAPs) and grouped the results in 11 fate differentiation categories. Among them, we identified 29 transcription factors (TFs) and 10 cell fate determinants. Significant differences were found in the molecular activities of vegetative and reproductive nuclei. The TFs in VN mainly participate in pollen tube development. In comparison, the TFs in GN are mainly involved in cell differentiation and male gametogenesis. The identified novel TFs may play an important role in cell fate differentiation. Our data also indicate differences in nuclear pore complexes and epigenetic modifications: more nucleoporins synthesized in VN; more histone variants and chaperones; and structural maintenance of chromosome (SMC) proteins, chromatin remodelers, and DNA methylation-related proteins expressed in GN. The VC has active macromolecular metabolism and mRNA processing, while GC has active nucleic acid metabolism and translation. Moreover, the members of unfolded protein response (UPR) and programmed cell death accumulate in VN, and DNA damage repair is active in GN. Differences in the stress response of DAPs in VN vs. GN were also found. This study provides a further understanding of pollen cell differentiation mechanisms and also a sound basis for future studies of the molecular mechanisms behind cell fate differentiation.

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Section: Differential Histone Programs Between Vn and Gn Mediated By Specific Histone Chaperonessupporting

confidence: 78%

Proteomic Analysis of Generative and Vegetative Nuclei Reveals Molecular Characteristics of Pollen Cell Differentiation in Lily

et al. 2021

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“…c). In our experiments, there were also some peptides from RuvB‐like protein 1, present in both SWR1 and INO80 complexes (Holt et al ., ), and components of the histone chaperone FACILITATES CHROMATIN TRANSCRIPTION (FACT) complex such as STRUCTURE‐SPECIFIC RECOGNITION PROTEIN 1 (SSRP1) and SUPPRESSOR OF Ty16 (SPT16) subunits (Zhou et al ., ; Pfab et al ., ). This complex is required for progression of transcribing RNA polymerase on chromatin templates via nucleosome destabilisation (Formosa, ).…”

Section: Resultsmentioning

confidence: 97%

Arabidopsis YAF9 histone readers modulate flowering time through NuA4‐complex‐dependent H4 and H2A.Z histone acetylation at FLC chromatin

et al. 2019

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Summary Posttranslational histone modifications and the dynamics of histone variant H2A.Z are key mechanisms underlying the floral transition. In yeast, SWR1‐C and NuA4‐C mediate the deposition of H2A.Z and the acetylation of histone H4, H2A and H2A.Z, respectively. Yaf9 is a subunit shared by both chromatin‐remodeling complexes. The significance of the two Arabidopsis YAF9 homologues, YAF9A and YAF9B, is unknown. To get an insight into the role of Arabidopsis YAF9 proteins in plant developmental responses, we followed physiological, genetic, genomic, epigenetic, proteomics and cell biology approaches. Our data revealed that YAF9A and YAF9B are histone H3 readers with unequally redundant functions. Double mutant yaf9a yaf9b plants display pleiotropic developmental phenotypic alterations as well as misregulation of a wide variety of genes. We demonstrated that YAF9 proteins regulate flowering time by both FLC‐dependent and independent mechanisms that work in parallel with SWR1‐C. Interestingly, we show that YAF9A binds FLC chromatin and that YAF9 proteins regulate FLC expression by modulating the acetylation levels of H2A.Z and H4 but not H2A.Z deposition. Our work highlights the key role exerted by YAF9 homologues in the posttranslational modification of canonical histones and variants that regulate gene expression in plants to control development.

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“…These experiments revealed that SSRP1 does not interact with DNA sequence-specifically, but according to a binding-site selection assay, it binds preferentially to sequences containing deformable dinucleotide steps (Röttgers et al, 2000). In line with this finding, mediated by its HMG-box domain SSRP1 can bend linear DNA and bind selectively to certain DNA structures (Röttgers et al, 2000;Pfab et al, 2018b). Furthermore, SSRP1 is phosphorylated by protein kinase CK2 and phosphorylation of two residues C-terminal of the HMG-box domain modulates the structure-specific interaction with DNA (Krohn et al, 2003).…”

Section: Basic Facts About Plant Factmentioning

confidence: 63%

“…In view of the relevance of the HMG-box domain for in vitro DNA/ nucleosome interactions, it was surprising that based on fluorescence recovery after photobleaching experiments intact SSRP1 and SSRP1 lacking its HMG-box domain (termed SSRP1ΔHMG) displayed the same mobility within nuclei of Arabidopsis cells. Beyond that, expression of SSRP1ΔHMG was almost as efficient as that of intact SSRP1 in supporting normal growth and development of the otherwise nonviable ssrp1-1 mutant (Pfab et al, 2018b). This suggested that the HMG-box domain, which is conserved among SSRP1 proteins of plants and metazoa, is not critical in Arabidopsis under standard growth conditions.…”

Section: Basic Facts About Plant Factmentioning

confidence: 99%

“…Furthermore, SSRP1 is phosphorylated by protein kinase CK2 and phosphorylation of two residues C-terminal of the HMG-box domain modulates the structure-specific interaction with DNA (Krohn et al, 2003). The HMG-box domain of SSRP1 is not only important for DNA-binding, but contributes also to nucleosome interactions (Lichota and Grasser, 2001;Pfab et al, 2018b). In view of the relevance of the HMG-box domain for in vitro DNA/ nucleosome interactions, it was surprising that based on fluorescence recovery after photobleaching experiments intact SSRP1 and SSRP1 lacking its HMG-box domain (termed SSRP1ΔHMG) displayed the same mobility within nuclei of Arabidopsis cells.…”

Section: Basic Facts About Plant Factmentioning

confidence: 99%

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The FACT Histone Chaperone: Tuning Gene Transcription in the Chromatin Context to Modulate Plant Growth and Development

Grasser

2020

Front. Plant Sci.

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FACT is a heterodimeric histone chaperone consisting of the SSRP1 and SPT16 proteins and is conserved among eukaryotes. It interacts with the histones H2A-H2B and H3-H4 as well as with DNA. Based on in vitro and in vivo studies mainly in yeast and mammalian cells, FACT can mediate nucleosome disassembly and reassembly and thus facilitates in the chromatin context DNA-dependent processes including transcription, replication and repair. In plants, primarily the role of FACT related to RNA polymerase II transcription has been examined. FACT was found to associate with elongating Arabidopsis RNA polymerase II (RNAPII) as part of the transcript elongation complex and it was identified as repressor of aberrant intragenic transcriptional initiation. Arabidopsis mutants depleted in FACT subunits exhibit various defects in vegetative and reproductive development. Strikingly, FACT modulates important developmental transitions by promoting expression of key repressors of these processes. Thus, FACT facilitates expression of DOG1 and FLC adjusting the switch from seed dormancy to germination and from vegetative to reproductive development, respectively. In the central cell of the female gametophyte, FACT can facilitate DNA demethylation especially within heterochromatin, and thereby contributes to gene imprinting during Arabidopsis reproduction. This review discusses results particularly from the plant perspective about the contribution of FACT to processes that involve reorganisation of nucleosomes with a main focus on RNAPII transcription and its implications for diverse areas of plant biology.

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The Arabidopsis Histone Chaperone FACT: Role of the HMG-Box Domain of SSRP1

Cited by 16 publications

References 61 publications

Proteomic Analysis of Generative and Vegetative Nuclei Reveals Molecular Characteristics of Pollen Cell Differentiation in Lily

Proteomic Analysis of Generative and Vegetative Nuclei Reveals Molecular Characteristics of Pollen Cell Differentiation in Lily

Arabidopsis YAF9 histone readers modulate flowering time through NuA4‐complex‐dependent H4 and H2A.Z histone acetylation at FLC chromatin

The FACT Histone Chaperone: Tuning Gene Transcription in the Chromatin Context to Modulate Plant Growth and Development

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