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Molecular and Cellular Biology, June 2004, p. 5391-5403, Vol. 24, No. 12
0270-7306/04/$08.00+0     DOI: 10.1128/MCB.24.12.5391-5403.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Histone mRNAs Do Not Accumulate during S Phase of either Mitotic or Endoreduplicative Cycles in the Chordate Oikopleura dioica

Mariacristina Chioda, Fabio Spada, Ragnhild Eskeland, and Eric M. Thompson^*

Sars International Centre for Marine Molecular Biology, Bergen High Technology Centre, N-5008 Bergen, Norway

Received 25 August 2003/ Returned for modification 1 December 2003/ Accepted 2 March 2004

Metazoan histones are generally classified as replication-dependent or replacement variants. Replication-dependent histone genes contain cell cycle-responsive promoter elements, their transcripts terminate in an unpolyadenylated conserved stem-loop, and their mRNAs accumulate sharply during S phase. Replacement variant genes lack cell cycle-responsive promoter elements, their polyadenylated transcripts lack the stem-loop, and they are expressed at low levels throughout the cell cycle. During early development of some organisms with rapid cleavage cycles, replication-dependent mRNAs are not fully S phase restricted until complete cell cycle regulation is achieved. The accumulation of polyadenylated transcripts during this period has been considered incompatible with metazoan development. We show here that histone metabolism in the urochordate Oikopleura dioica does not accord with some key tenets of the replication-dependent/replacement variant paradigm. During the premetamorphic mitotic phase of development, expressed variants shared characteristics of replication-dependent histones, including the 3' stem-loop, but, in contrast, were extensively polyadenylated. After metamorphosis, when cells in many tissues enter endocycles, there was a global downregulation of histone transcript levels, with most variant transcripts processed at the stem-loop. Contrary to the 30-fold S-phase upregulation of histone transcripts described in common metazoan model organisms, we observed essentially constant histone transcript levels throughout both mitotic and endoreduplicative cell cycles.

Present address: Adolf-Butenandt Institut, Ludwig Maximillians University of Munich, Munich, Germany.

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• Fu, X., Adamski, M., Thompson, E. M. (2008). Altered miRNA Repertoire in the Simplified Chordate, Oikopleura dioica. Mol Biol Evol 25: 1067-1080 [Abstract] [Full Text]