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Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell

Nature Plants volume 2, Article number: 16030 (2016) Cite this article

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Abstract

Plant small interfering RNAs (siRNAs) communicate from cell to cell and travel long distances through the vasculature. However, siRNA movement into germ cells has remained controversial, and has gained interest because the terminally differentiated pollen vegetative nurse cell surrounding the sperm cells undergoes a programmed heterochromatin decondensation and transcriptional reactivation of transposable elements (TEs). Transcription of TEs leads to their post-transcriptional degradation into siRNAs, and it has been proposed that the purpose of this TE reactivation is to generate and load TE siRNAs into the sperm cells. Here, we identify the molecular pathway of TE siRNA production in the pollen grain and demonstrate that siRNAs produced from pollen vegetative cell transcripts can silence TE reporters in the sperm cells. Our data demonstrates that TE siRNAs act non-cell-autonomously, inhibiting TE activity in the germ cells and potentially the next generation.

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Figure 1: TE siRNA-mediated silencing in the pollen vegetative cell.
Figure 2: Pollen TE siRNA-mediated regulation is dependent on AGO1, AGO2 and DCL4.
Figure 3: Transitive small RNA silencing between the pollen vegetative cell and sperm cells.
Figure 4: Inhibition of vegetative cell siRNAs results in TE transcript regulation in the sperm cells.

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Acknowledgements

The authors thank C. DeFraia for his data contributions, F. Qu for the 2b clone and J. Daron for assistance with data analysis. The authors also thank A. Dobritsa, A. McCue, M. Mirouze and X. Zhou for their comments. G.M. is supported by a Marie Curie IOF Postdoctoral Fellowship (PIOF-GA-2012-330069). This research was supported by NSF grants MCB-1020499 and MCB-1252370 to R.K.S.

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Author notes

  1. Germán Martínez

    Present address: †Present address: Department of Plant Biology, Swedish University of Agricultural Sciences and Linnean Center of Plant Biology, Uppsala, Sweden.,

Authors and Affiliations

  1. Department of Molecular Genetics and Center for RNA Biology, The Ohio State University, 500 Aronoff Laboratory, 318 West 12th Avenue, Columbus, 43210, Ohio, USA

    Germán Martínez, Kaushik Panda & R. Keith Slotkin

  2. Department of Plant Biology, Swedish University of Agricultural Sciences and Linnean Center of Plant Biology, SE-750 07 Uppsala, Sweden

    Claudia Köhler

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Contributions

G.M. and R.K.S. devised the experimental approach. G.M. performed the experimental work, generated transgenic lines, sequencing libraries and performed the data analysis. K.P. analysed the small RNA data. R.K.S, C.K. and G.M. wrote the paper.

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Correspondence to R. Keith Slotkin.

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Martínez, G., Panda, K., Köhler, C. et al. Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell. Nature Plants 2, 16030 (2016). https://doi.org/10.1038/nplants.2016.30

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