Originally published as Genetics Published Articles Ahead of Print on September 30, 2004.

Genetics, Vol. 169, 149-160, January 2005, Copyright © 2005
doi:10.1534/genetics.104.032300

Communication Between Parental and Developing Genomes During Tetrahymena Nuclear Differentiation Is Likely Mediated by Homologous RNAs

Douglas L. Chalker^*,1, Patrick Fuller and Meng-Chao Yao^,

^* Department of Biology, Washington University, Saint Louis, Missouri 63130
Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington 98109
Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan 11529, Republic of China

¹ Corresponding author: Department of Biology, Campus Box 1137, Washington University, One Brookings Dr., St. Louis, MO 63130.
E-mail: dchalker{at}biology2.wustl.edu

Approximately 6000 DNA elements, totaling nearly 15 Mb, are coordinately excised from the developing somatic genome of Tetrahymena thermophila. An RNA interference (RNAi)-related mechanism has been implicated in the targeting of these germline-limited sequences for chromatin modification and subsequent DNA rearrangement. The excision of individual DNA segments can be inhibited if the homologous sequence is placed within the parental somatic nucleus, indicating that communication occurs between the parental and developing genomes. To determine how the DNA content of one nucleus is communicated to the other, we assessed DNA rearrangement occurring in wild-type cells that were mated to cells that contained the normally germline-limited M element within their somatic nuclei. M-element rearrangement was blocked in the wild-type cell even when no genetic exchange occurred between mating partners, a finding that is inconsistent with any genetic imprinting models. This inhibition by the parental somatic nucleus was rapidly established between 5 and 6 hr of conjugation, near or shortly after the time that zygotic nuclei are formed. M-element small RNAs (sRNAs) that are believed to direct its rearrangement were found to rapidly accumulate during the first few hours of conjugation before stabilizing to a low, steady-state level. The period between 5 and 6 hr during which sRNA levels stabilize correlates with the time after which the parental genome can block DNA rearrangement. These data lead us to suggest that homologous sRNAs serve as mediators to communicate sequence-specific information between the parental and developing genomes, thereby regulating genome-wide DNA rearrangement, and that these sRNAs can be effectively compared to the somatic genome of both parents.

This article has been cited by other articles:

				G. Lepere, M. Nowacki, V. Serrano, J.-F. Gout, G. Guglielmi, S. Duharcourt, and E. Meyer Silencing-associated and meiosis-specific small RNA pathways in Paramecium tetraurelia Nucleic Acids Res., February 1, 2009; 37(3): 903 - 915. [Abstract] [Full Text] [PDF]

				A. Gratias, G. Lepere, O. Garnier, S. Rosa, S. Duharcourt, S. Malinsky, E. Meyer, and M. Betermier Developmentally programmed DNA splicing in Paramecium reveals short-distance crosstalk between DNA cleavage sites Nucleic Acids Res., June 1, 2008; 36(10): 3244 - 3251. [Abstract] [Full Text] [PDF]

				G. Lepere, M. Betermier, E. Meyer, and S. Duharcourt Maternal noncoding transcripts antagonize the targeting of DNA elimination by scanRNAs in Paramecium tetraurelia Genes & Dev., June 1, 2008; 22(11): 1501 - 1512. [Abstract] [Full Text] [PDF]

				T. Robinson and L. A. Katz Non-Mendelian Inheritance of Paralogs of 2 Cytoskeletal Genes in the Ciliate Chilodonella uncinata Mol. Biol. Evol., November 1, 2007; 24(11): 2495 - 2503. [Abstract] [Full Text] [PDF]

				Y. Liu, S. D. Taverna, T. L. Muratore, J. Shabanowitz, D. F. Hunt, and C. D. Allis RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena Genes & Dev., June 15, 2007; 21(12): 1530 - 1545. [Abstract] [Full Text] [PDF]

				M.-C. Yao, C.-H. Yao, L. M. Halasz, P. Fuller, C. H. Rexer, S. H. Wang, R. Jain, R. S. Coyne, and D. L. Chalker Identification of novel chromatin-associated proteins involved in programmed genome rearrangements in Tetrahymena J. Cell Sci., June 15, 2007; 120(12): 1978 - 1989. [Abstract] [Full Text] [PDF]

				R. A. Howard-Till and M.-C. Yao Induction of Gene Silencing by Hairpin RNA Expression in Tetrahymena thermophila Reveals a Second Small RNA Pathway Mol. Cell. Biol., December 1, 2006; 26(23): 8731 - 8742. [Abstract] [Full Text] [PDF]

				C. A. Kowalczyk, A. M. Anderson, M. Arce-Larreta, and D. L. Chalker The germ line limited M element of Tetrahymena is targeted for elimination from the somatic genome by a homology-dependent mechanism Nucleic Acids Res., November 6, 2006; 34(20): 5778 - 5789. [Abstract] [Full Text] [PDF]

				R. A. Zufall, C. L. McGrath, S. V. Muse, and L. A. Katz Genome Architecture Drives Protein Evolution in Ciliates Mol. Biol. Evol., September 1, 2006; 23(9): 1681 - 1687. [Abstract] [Full Text] [PDF]

				S. R. Lee and K. Collins Two classes of endogenous small RNAs in Tetrahymena thermophila Genes & Dev., January 1, 2006; 20(1): 28 - 33. [Abstract] [Full Text] [PDF]

				C. D. Malone, A. M. Anderson, J. A. Motl, C. H. Rexer, and D. L. Chalker Germ Line Transcripts Are Processed by a Dicer-Like Protein That Is Essential for Developmentally Programmed Genome Rearrangements of Tetrahymena thermophila Mol. Cell. Biol., October 15, 2005; 25(20): 9151 - 9164. [Abstract] [Full Text] [PDF]

International Access Link

Online ISSN: 1943-2361  Print ISSN: 0016-6731
Copyright 2009 by the Genetics Society of America
phone: 412-268-1812   fax: 412-268-1813   email: genetics-gsa{at}andrew.cmu.edu