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Plant Physiol. 2018 Apr;176(4):2700-2719. doi: 10.1104/pp.17.01828. Epub 2018 Feb 8.

A Genetic Network for Systemic RNA Silencing in Plants.

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Research Centre for Plant RNA Signaling, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 310036, China.
Warwick-Hangzhou RNA Signaling Joint Laboratory, School of Life Sciences, University of Warwick, Warwick CV4 7AL, United Kingdom.
Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China.
Centre for Plant Biology and MOE Key Laboratory of Bioinformatics, School of Life Sciences, Tsinghua University, Beijing 100084, China.
UMR EGFV, Bordeaux Sciences Agro, INRA, Université de Bordeaux, 210 Chemin de Leysotte, CS 50008, 33882 Villenave d'Ornon, France.
Research Centre for Plant RNA Signaling, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 310036, China
Worcester-Hangzhou Joint Molecular Plant Health Laboratory, Institute of Science and the Environment, University of Worcester, WR2 6AJ, United Kingdom.


Non-cell autonomous RNA silencing can spread from cell to cell and over long distances in animals and plants. However, the genetic requirements and signals involved in plant mobile gene silencing are poorly understood. Here, we identified a DICER-LIKE2 (DCL2)-dependent mechanism for systemic spread of posttranscriptional RNA silencing, also known as posttranscriptional gene silencing (PTGS), in Nicotiana benthamiana Using a suite of transgenic DCL RNAi lines coupled with a GFP reporter, we demonstrated that N. benthamiana DCL1, DCL2, DCL3, and DCL4 are required to produce microRNAs and 22, 24, and 21nt small interfering RNAs (siRNAs), respectively. All investigated siRNAs produced in local incipient cells were present at low levels in distal tissues. Inhibition of DCL2 expression reduced the spread of gene silencing, while suppression of DCL3 or DCL4 expression enhanced systemic PTGS. In contrast to DCL4 RNAi lines, DCL2-DCL4 double-RNAi lines developed systemic PTGS similar to that observed in DCL2 RNAi. We further showed that the 21 or 24 nt local siRNAs produced by DCL4 or DCL3 were not involved in long-distance gene silencing. Grafting experiments demonstrated that DCL2 was required in the scion to respond to the signal, but not in the rootstock to produce/send the signal. These results suggest a coordinated DCL genetic pathway in which DCL2 plays an essential role in systemic PTGS in N. benthamiana, while both DCL4 and DCL3 attenuate systemic PTGS. We discuss the potential role of 21, 22, and 24 nt siRNAs in systemic PTGS.

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