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Molecular and Cellular Biology, April 2007, p. 2648-2660, Vol. 27, No. 7
0270-7306/07/$08.00+0     doi:10.1128/MCB.01910-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Phosphorylation of the SQ H2A.X Motif Is Required for Proper Meiosis and Mitosis in Tetrahymena thermophila{triangledown}

Xiaoyuan Song,1,{dagger},{ddagger} Elizabeta Gjoneska,2,{dagger} Qinghu Ren,1,{dagger},§ Sean D. Taverna,2 C. David Allis,2 and Martin A. Gorovsky1*

Department of Biology, University of Rochester, Rochester, New York,1 Laboratory of Chromatin Biology, Rockefeller University, New York, New York2

Received 9 October 2006/ Returned for modification 30 November 2006/ Accepted 8 January 2007

Phosphorylation of the C terminus SQ motif that defines H2A.X variants is required for efficient DNA double-strand break (DSB) repair in diverse organisms but has not been studied in ciliated protozoa. Tetrahymena H2A.X is one of two similarly expressed major H2As, thereby differing both from mammals, where H2A.X is a quantitatively minor component, and from Saccharomyces cerevisiae where it is the only type of major H2A. Tetrahymena H2A.X is phosphorylated in the SQ motif in both the mitotic micronucleus and the amitotic macronucleus in response to DSBs induced by chemical agents and in the micronucleus during prophase of meiosis, which occurs in the absence of a synaptonemal complex. H2A.X is phosphorylated when programmed DNA rearrangements occur in developing macronuclei, as for immunoglobulin gene rearrangements in mammals, but not during the DNA fragmentation that accompanies breakdown of the parental macronucleus during conjugation, correcting the previous interpretation that this process is apoptosis-like. Using strains containing a mutated (S134A) SQ motif, we demonstrate that phosphorylation of this motif is important for Tetrahymena cells to recover from exogenous DNA damage and is required for normal micronuclear meiosis and mitosis and, to a lesser extent, for normal amitotic macronuclear division; its absence, while not lethal, leads to the accumulation of DSBs in both micro- and macronuclei. These results demonstrate multiple roles of H2A.X phosphorylation in maintaining genomic integrity in different phases of the Tetrahymena life cycle.

* Corresponding author. Mailing address: Department of Biology, University of Rochester, Rochester, NY 14627. Phone: (585) 275-6988. Fax: (585) 275-2070. E-mail: goro{at}mail.rochester.edu.

{triangledown} Published ahead of print on 22 January 2007.

{ddagger} Present address: School of Medicine, University of California—San Diego, La Jolla, CA 92037.

{dagger} X.S., E.G., and Q.R. were equal contributors to this paper.

§ Present address: The Institute for Genomic Research, Rockville, MD 20850.

Molecular and Cellular Biology, April 2007, p. 2648-2660, Vol. 27, No. 7
0270-7306/07/$08.00+0     doi:10.1128/MCB.01910-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Loidl, J., Mochizuki, K. (2009). Tetrahymena Meiotic Nuclear Reorganization Is Induced by a Checkpoint Kinase-dependent Response to DNA Damage. Mol. Biol. Cell 20: 2428-2437 [Abstract] [Full Text]  
  • Mochizuki, K., Novatchkova, M., Loidl, J. (2008). DNA double-strand breaks, but not crossovers, are required for the reorganization of meiotic nuclei in Tetrahymena. J. Cell Sci. 121: 2148-2158 [Abstract] [Full Text]  


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