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Science 11 February 2005:
Vol. 307. no. 5711, pp. 932 - 935
DOI: 10.1126/science.1107130

Reports

Methylation as a Crucial Step in Plant microRNA Biogenesis

Bin Yu,* Zhiyong Yang,* Junjie Li,{dagger} Svetlana Minakhina, Maocheng Yang, Richard W. Padgett, Ruth Steward, Xuemei Chen{ddagger}

Methylation on the base or the ribose is prevalent in eukaryotic ribosomal RNAs (rRNAs) and is thought to be crucial for ribosome biogenesis and function. Artificially introduced 2'-O-methyl groups in small interfering RNAs (siRNAs) can stabilize siRNAs in serum without affecting their activities in RNA interference in mammalian cells. Here, we show that plant microRNAs (miRNAs) have a naturally occurring methyl group on the ribose of the last nucleotide. Whereas methylation of rRNAs depends on guide RNAs, the methyltransferase protein HEN1 is sufficient to methylate miRNA/miRNA* duplexes. Our studies uncover a new and crucial step in plant miRNA biogenesis and have profound implications in the function of miRNAs.

Waksman Institute, Rutgers University, Piscataway, NJ 08854, USA.

* These authors contributed equally to this work.

{dagger} Present address: Howard Hughes Medical Institute and Skirball Institute of Biomolecular Medicine, New York University School of Medicine, 540 First Avenue, Skirball 2-17, New York, NY 10016, USA.

{ddagger} To whom correspondence should be addressed. E-mail: xuemei{at}waksman.rutgers.edu

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   Abstract »    Full Text »    PDF »
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