The Histone Chaperone NRP1 Interacts with WEREWOLF to Activate GLABRA2 in Arabidopsis Root Hair Development

• Published in: The Plant cell 2017-02, Vol.29 (2), p.260-276
• Main Authors: Zhu, Yan, Rong, Liang, Luo, Qiang, Wang, Baihui, Zhou, Nana, Yang, Yue, Zhang, Chi, Feng, Haiyang, Zheng, Lina, Shen, Wen-Hui, Ma, Jinbiao, Dong, Aiwu
• Format: Article
• Language: English
• Subjects: Arabidopsis; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - metabolism; Arabidopsis Proteins - chemistry; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis Proteins - physiology; Arabidopsis thaliana; Biochemistry, Molecular Biology; Cellular Biology; Chaperones; Chromatin; Crystallography; Deoxyribonucleic acid; Dimerization; DNA; DNA-Binding Proteins - genetics; DNA-Binding Proteins - metabolism; DNA-Binding Proteins - physiology; Gene Expression Regulation, Plant; Histones; Histones - metabolism; Histones - physiology; Homeodomain Proteins - genetics; Homeodomain Proteins - metabolism; Homeodomain Proteins - physiology; Life Sciences; Molecular biology; Molecular modelling; Phenotypes; Plant Roots - genetics; Plant Roots - growth & development; Plant Roots - metabolism; Promoter Regions, Genetic; Root hairs; Transcription factors; Vegetal Biology
• ISSN: 1040-4651; 1532-298X; 1532-298X
• DOI: 10.1105/tpc.16.00719

NUCLEOSOME ASSEMBLY PROTEIN1 (NAP1) defines an evolutionarily conserved family of histone chaperones and loss of function of the Arabidopsis thaliana NAP1 family genes NAP1-RELATED PROTEIN1 (NRP1) and NRP2 causes abnormal root hair formation. Yet, the underlying molecular mechanisms remain unclear. Here, we show that NRP1 interacts with the transcription factor WEREWOLF (WER) in vitro and in vivo and enriches at the GLABRA2 (GL2) promoter in a WER-dependent manner. Crystallographic analysis indicates that NRP1 forms a dimer via its N-terminal α-helix. Mutants of NRP1 that either disrupt the α-helix dimerization or remove the C-terminal acidic tail, impair its binding to histones and WER and concomitantly lead to failure to activate GL2 transcription and to rescue the nrp1-1 nrp2-1 mutant phenotype. Our results further demonstrate that WER-dependent enrichment of NRP1 at the GL2 promoter is involved in local histone eviction and nucleosome loss in vivo. Biochemical competition assays imply that the association between NRP1 and histones may counteract the inhibitory effect of histones on the WER-DNA interaction. Collectively, our study provides important insight into the molecular mechanisms by which histone chaperones are recruited to target chromatin via interaction with a genespecific transcription factor to moderate chromatin structure for proper root hair development.