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Vol. 19, Issue 3, 1162-1173, March 2008

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Distinct Chromatin Modulators Regulate the Formation of Accessible and Repressive Chromatin at the Fission Yeast Recombination Hotspot ade6-M26

Kouji Hirota^*,, Ken-ichi Mizuno, Takehiko Shibata^*,, and Kunihiro Ohta^*,

*Shibata Distinguished Senior Scientist Laboratory, RIKEN Discovery Research Institute, Wako-shi, Saitama 351-0198, Japan; Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Komaba, Tokyo 153-8902, Japan; Genome Damage and Stability Centre, University of Sussex, Brighton BN1 9RQ, United Kingdom; and Division of Molecular and Cellular Physiology, International Graduate School of Arts and Sciences, Yokohama City University, Yokohama, Kanagawa 230-0045, Japan

Submitted April 25, 2007; Revised December 17, 2007; Accepted January 4, 2007
Monitoring Editor: Wendy Bickmore

Histone acetyltransferases (HATs) and ATP-dependent chromatin remodeling factors (ADCRs) regulate transcription and recombination via alteration of local chromatin configuration. The ade6-M26 allele of Schizosaccharomyces pombe creates a meiotic recombination hotspot that requires a cAMP-responsive element (CRE)-like sequence M26, the Atf1/Pcr1 heterodimeric ATF/CREB transcription factor, the Gcn5 HAT, and the Snf22 SWI2/SNF2 family ADCR. Chromatin alteration occurs meiotically around M26, leading to the activation of meiotic recombination. We newly report the roles of other chromatin remodeling factors that function positively and negatively in chromatin alteration at M26: two CHD-1 family ADCRs (Hrp1 and Hrp3), a Spt-Ada-Gcn5 acetyltransferase component (Ada2), and a member of Moz-Ybf2/Sas3-Sas2-Tip60 family (Mst2). Ada2, Mst2, and Hrp3 are required for the full activation of chromatin changes around M26 and meiotic recombination. Acetylation of histone H3 around M26 is remarkably reduced in gcn5, ada2 and snf22, suggesting cooperative functions of these HAT complexes and Snf22. Conversely, Hrp1, another CHD-1 family ADCR, maintains repressive chromatin configuration at ade6-M26. Interestingly, transcriptional initiation site is shifted to a site around M26 from the original initiation sites, in couple with the histone acetylation and meiotic chromatin alteration induced around 3' region of M26, suggesting a collaboration between these chromatin modulators and the transcriptional machinery to form accessible chromatin. These HATs and ADCRs are also required for the regulation of transcription and chromatin structure around M26 in response to osmotic stress. Thus, we propose that multiple chromatin modulators regulate chromatin structure reversibly and participate in the regulation of both meiotic recombination and stress-induced transcription around CRE-like sequences.

Address correspondence to: Kouji Hirota (khirota{at}postman.riken.jp)

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