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Genomic and Genetic Characterization of Rice Cen3 Reveals Extensive Transcription and Evolutionary Implications of a Complex Centromere^[W],[OA]

^a Department of Horticulture, University of Wisconsin, Madison, Wisconsin 53706
^b Department of Plant and Soil Sciences, Delaware Biotechnology Institute, University of Delaware, Newark, Delaware 19711
^c The Institute for Genomic Research, Rockville, Maryland 20850
^d Department of Plant Pathology, University of Wisconsin, Madison, Wisconsin 53706
^e Department of Plant Pathology, The Ohio State University, Columbus, Ohio 43210
^f Department of Plant Sciences, BIO5 Institute, University of Arizona, Tucson, Arizona 85721

² To whom correspondence should be addressed. E-mail jjiang1{at}wisc.edu; fax 608-262-4743.

The centromere is the chromosomal site for assembly of the kinetochore where spindle fibers attach during cell division. In most multicellular eukaryotes, centromeres are composed of long tracts of satellite repeats that are recalcitrant to sequencing and fine-scale genetic mapping. Here, we report the genomic and genetic characterization of the complete centromere of rice (Oryza sativa) chromosome 3. Using a DNA fiber-fluorescence in situ hybridization approach, we demonstrated that the centromere of chromosome 3 (Cen3) contains 441 kb of the centromeric satellite repeat CentO. Cen3 includes an 1,881-kb domain associated with the centromeric histone CENH3. This CENH3-associated chromatin domain is embedded within a 3113-kb region that lacks genetic recombination. Extensive transcription was detected within the CENH3 binding domain based on comprehensive annotation of protein-coding genes coupled with empirical measurements of mRNA levels using RT-PCR and massively parallel signature sequencing. Genes <10 kb from the CentO satellite array were expressed in several rice tissues and displayed histone modification patterns consistent with euchromatin, suggesting that rice centromeric chromatin accommodates normal gene expression. These results support the hypothesis that centromeres can evolve from gene-containing genomic regions.

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