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Open Access Research article

Mutation of the RDR1 gene caused genome-wide changes in gene expression, regional variation in small RNA clusters and localized alteration in DNA methylation in rice

Ningning Wang125, Di Zhang1, Zhenhui Wang1, Hongwei Xun1, Jian Ma2, Hui Wang1, Wei Huang1, Ying Liu1, Xiuyun Lin3, Ning Li1, Xiufang Ou1, Chunyu Zhang14, Ming-Bo Wang5 and Bao Liu1*

Author Affiliations

1 Key Laboratory of Molecular Epigenetics of Ministry of Education (MOE), Northeast Normal University, Changchun 130024, China

2 Faculty of Agronomy, Jilin Agricultural University, Changchun 130118, China

3 Jilin Academy of Agricultural Sciences, Changchun 130033, China

4 School of Food Production Technology and Biotechnology, Changchun Vocational Institute of Technology, Changchun, China

5 Commonwealth Scientific and Industrial Research Organisation Plant Industry, Canberra, Australian Capital Territory 2601, Australia

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BMC Plant Biology 2014, 14:177  doi:10.1186/1471-2229-14-177

Published: 30 June 2014

Abstract

Background

Endogenous small (sm) RNAs (primarily si- and miRNAs) are important trans/cis-acting regulators involved in diverse cellular functions. In plants, the RNA-dependent RNA polymerases (RDRs) are essential for smRNA biogenesis. It has been established that RDR2 is involved in the 24 nt siRNA-dependent RNA-directed DNA methylation (RdDM) pathway. Recent studies have suggested that RDR1 is involved in a second RdDM pathway that relies mostly on 21 nt smRNAs and functions to silence a subset of genomic loci that are usually refractory to the normal RdDM pathway in Arabidopsis. Whether and to what extent the homologs of RDR1 may have similar functions in other plants remained unknown.

Results

We characterized a loss-of-function mutant (Osrdr1) of the OsRDR1 gene in rice (Oryza sativa L.) derived from a retrotransposon Tos17 insertion. Microarray analysis identified 1,175 differentially expressed genes (5.2% of all expressed genes in the shoot-tip tissue of rice) between Osrdr1 and WT, of which 896 and 279 genes were up- and down-regulated, respectively, in Osrdr1. smRNA sequencing revealed regional alterations in smRNA clusters across the rice genome. Some of the regions with altered smRNA clusters were associated with changes in DNA methylation. In addition, altered expression of several miRNAs was detected in Osrdr1, and at least some of which were associated with altered expression of predicted miRNA target genes. Despite these changes, no phenotypic difference was identified in Osrdr1 relative to WT under normal condition; however, ephemeral phenotypic fluctuations occurred under some abiotic stress conditions.

Conclusions

Our results showed that OsRDR1 plays a role in regulating a substantial number of endogenous genes with diverse functions in rice through smRNA-mediated pathways involving DNA methylation, and which participates in abiotic stress response.

Keywords:
Gene expression; Epigenetics; Small RNA; DNA methylation; RDR1; Oryza sativa L