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Transposon-derived small RNA is responsible for modified function of WRKY45 locus

Nature Plants volume 2, Article number: 16016 (2016) Cite this article

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Abstract

Transposable elements (TEs) are an important source for generating small interfering RNAs (siRNAs) in plants and animals. Although TE-siRNA-induced silencing of TEs by RNA-directed DNA methylation (RdDM) in the maintenance of genome integrity has been intensively studied, it is unknown whether this type of silencing occurs in suppressing endogenous non-TE genes during host–pathogen interactions. Here we show that a TE-siRNA, TE-siR815, causes opposite functions for the two alleles, WRKY45-1 and WRKY45-2, of the WRKY45 transcription factor in rice resistance to Xanthomonas oryzae pv. oryzae, which causes the most devastating bacterial disease in rice worldwide. Expression of WRKY45-1, but not WRKY45-2, generated TE-siR815, which in turn repressed ST1, an important component in WRKY45-mediated resistance, by RdDM. Suppression of ST1 abolished WRKY45-mediated resistance leading to pathogen susceptibility. These results suggest that TE-siR815 contributes to the natural variation of the WRKY45 locus and TE-siR815-induced suppression of ST1 results in the negative role of WRKY45-1 but positive role of WRKY45-2 in regulating disease resistance.

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Figure 1: Rice TE-derived sRNA TE-siR815/osa-miR815.
Figure 2: TE-siR815 expression was associated with WRKY45-1 expression in leaves.
Figure 3: Overexpressing WRKY45-1.2 enhanced resistance to Xoo PXO61.
Figure 4: Overexpressing TE-siR815b blocked WRKY45-1.2- and WRKY45-2-mediated resistance.
Figure 5: Transcriptional activation of ST1 was associated with WRKY45-2-mediated resistance.
Figure 6: OsRDR2 and OsDCL3a influenced the generation of TE-siR815 and methylation of ST1.

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Acknowledgements

We thank Y. Qi (Tsinghua University), X. Cao (the Institute of Genetics and Developmental Biology), G. An (Kyung Hee University) and D. Zhou (Huazhong Agricultural University) for kindly providing rice seeds, RDR2, DCL and DRM2 RNAi lines or mutants and the sRNA PAGE–northern protocol. We also thank C. Zhou for help with DNA methylation analysis. This work was supported by grants from the National Natural Science Foundation of China (grant nos 31471757 and 31200912) and the National Program on the Development of Basic Research in China (grant no. 2012CB114005).

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Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan, 430070, China

    Haitao Zhang, Zeng Tao, Hanming Hong, Zhihui Chen, Changyin Wu, Xianghua Li, Jinghua Xiao & Shiping Wang

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  1. Haitao Zhang
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Contributions

H.Z. designed the study, conducted most of the experiments, analysed the data and drafted the manuscript; Z.T., H.H., Z.C. and C.W. helped to generate some transgenic plants and small RNA sequencing; J.X. and X.L. provided biochemical and molecular analysis support and management; and S.W. designed and supervised the study, interpreted data and revised the manuscript. All authors read and approved the manuscript.

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Correspondence to Shiping Wang.

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Zhang, H., Tao, Z., Hong, H. et al. Transposon-derived small RNA is responsible for modified function of WRKY45 locus. Nature Plants 2, 16016 (2016). https://doi.org/10.1038/nplants.2016.16

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