Histone chaperone ASF1 is involved in gene transcription activation in response to heat stress in Arabidopsis thaliana

Abstract

ANTI-SILENCING FUNCTION 1 (ASF1) is an evolutionarily conserved histone chaperone involved in diverse chromatin-based processes in eukaryotes. Yet, its role in transcription and the underlying molecular mechanisms remain largely elusive, particularly in plants. Here, we show that the Arabidopsis thaliana ASF1 homologous genes, AtASF1A and AtASF1B, are involved in gene transcription activation in response to heat stress. The Atasf1ab mutant displays defective basal as well as acquired thermotolerance phenotypes. Heat-induced expression of several key genes, including the HEAT SHOCK PROTEIN (HSP) genes Hsp101, Hsp70, Hsa32, Hsp17.6A and Hsp17.6B-CI, and the HEAT SHOCK FACTOR (HSF) gene HsfA2 but not HsfB1 is drastically impaired in Atasf1ab as compared with that in wild type. We found that AtASF1A/B proteins are recruited onto chromatin, and their enrichment is correlated with nucleosome removal and RNA polymerase II accumulation at the promoter and coding regions of HsfA2 and Hsa32 but not HsfB1. Moreover, AtASF1A/B facilitate H3K56 acetylation (H3K56ac), which is associated with HsfA2 and Hsa32 activation. Taken together, our study unravels an important function of AtASF1A/B in plant heat stress response and suggests that AtASF1A/B participate in transcription activation of some but not all HSF and HSP genes via nucleosome removal and H3K56ac stimulation.

Distinct roles of the histone chaperones NAP1 and NRP and the chromatin‐remodeling factor INO80 in somatic homologous recombination in Arabidopsis thaliana

“…Furthermore, in human cell lines, while NAP1 positively regulates HR (Machida et al, 2014), SET/TAF-I/I 2 PP2A /INHAT has recently been reported to play a repressor role in HR and the DNA damage response (Kalousi et al, 2015). Our finding of a non-essential role of AtNAP1 and NRP in plant growth and development also contrasts with the drastic and pleiotropic growth and developmental defects described for mutants of other types of histone chaperones, including CHROMATIN ASSEMBLY FACTOR-1 (CAF-1; Kaya et al, 2001), ANTI-SILENCING FUNCTION1 (ASF1; Zhu et al, 2011;Lario et al, 2013;Weng et al, 2014) and FACILITATES CHROMATIN TRANSCRIPTION (FACT; Lolas et al, 2010). CAF-1 and ASF1 are considered as H3/H4-type histone chaperones whereas FACT is classified as an H2A/ H2B-type histone chaperone (Avvakumov et al, 2011;Zhu et al, 2012).…”

“…Our finding of a non‐essential role of AtNAP1 and NRP in plant growth and development also contrasts with the drastic and pleiotropic growth and developmental defects described for mutants of other types of histone chaperones, including CHROMATIN ASSEMBLY FACTOR‐1 (CAF‐1; Kaya et al ., ), ANTI‐SILENCING FUNCTION1 (ASF1; Zhu et al ., ; Lario et al ., ; Weng et al ., ) and FACILITATES CHROMATIN TRANSCRIPTION (FACT; Lolas et al ., ). CAF‐1 and ASF1 are considered as H3/H4‐type histone chaperones whereas FACT is classified as an H2A/H2B‐type histone chaperone (Avvakumov et al ., ; Zhu et al ., ).…”

Stress-induced structural changes in plant chromatin

“…Vice versa, genes encoding stress-responsive proteins are up-regulated in mutants lacking CAF-1 or ANTI-SILENCING FUNCTION 1 (ASF1) proteins, other H3/H4 chaperones [64 ,65]. Plants expressing a truncated NUCLEOSOME ASSEMBLY PROTEIN 1 (NAP1), an H2A-H2B chaperone [66], or lacking ASF1 [64 ] show hypersensitivity to stress. ASF1 proteins bind directly to certain heat shock genes in a stress-dependent manner, where they may facilitate nucleosome dissociation and gene activation [64 ].…”

The H3 chaperone function of NASP is conserved in Arabidopsis

“…In Arabidopsis, CAF-1 is understood best (Kaya et al, 2001;Exner et al, 2006Exner et al, , 2008Kirik et al, 2006;Ono et al, 2006;Sch€ onrock et al, 2006;Ramirez-Parra and Gutierrez, 2007;Abe et al, 2008;Mozgova et al, 2010;Jaske et al, 2013;Muchova et al, 2015). In addition, the H3-chaperones ASF1 and HIRA have been described in plants (Phelps-Durr et al, 2005;Zhu et al, 2011;Lario et al, 2013;Nie et al, 2014;Weng et al, 2014;Duc et al, 2015). FACT and NAP1-type H2A-H2B chaperones are also conserved between plants and animals (Duroux et al, 2004;Galichet and Gruissem, 2006;Zhu et al, 2006;Liu et al, 2009a,b;Lolas et al, 2010;Gao et al, 2012).…”