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      Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection

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          Abstract

          Aggressive fungal pathogens such as Botrytis and Verticillium spp. cause severe crop losses worldwide. We recently discovered that Botrytis cinerea delivers small RNAs ( Bc-sRNAs) into plant cells to silence host immunity genes. Such sRNA effectors are mostly produced by B. cinerea Dicer-like protein 1 (Bc-DCL1) and Bc-DCL2. Here we show that expressing sRNAs that target Bc-DCL1 and Bc-DCL2 in Arabidopsis and tomato silences Bc-DCL genes and attenuates fungal pathogenicity and growth, exemplifying bidirectional cross-kingdom RNAi and sRNA trafficking between plants and fungi. This strategy can be adapted to simultaneously control multiple fungal diseases. We also show that Botrytis can take up external sRNAs and double-stranded RNAs (dsRNAs). Applying sRNAs or dsRNAs that target Botrytis DCL1 and DCL2 genes on the surface of fruits, vegetables, and flowers significantly inhibits gray mold disease. Such pathogen gene-targeting RNAs represent a new generation of environmentally-friendly fungicides.

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          Most cited references42

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          Small silencing RNAs: an expanding universe.

          Since the discovery in 1993 of the first small silencing RNA, a dizzying number of small RNA classes have been identified, including microRNAs (miRNAs), small interfering RNAs (siRNAs) and Piwi-interacting RNAs (piRNAs). These classes differ in their biogenesis, their modes of target regulation and in the biological pathways they regulate. There is a growing realization that, despite their differences, these distinct small RNA pathways are interconnected, and that small RNA pathways compete and collaborate as they regulate genes and protect the genome from external and internal threats.
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            RNA silencing in plants.

            There are at least three RNA silencing pathways for silencing specific genes in plants. In these pathways, silencing signals can be amplified and transmitted between cells, and may even be self-regulated by feedback mechanisms. Diverse biological roles of these pathways have been established, including defence against viruses, regulation of gene expression and the condensation of chromatin into heterochromatin. We are now in a good position to investigate the full extent of this functional diversity in genetic and epigenetic mechanisms of genome control.
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              Control of coleopteran insect pests through RNA interference.

              Commercial biotechnology solutions for controlling lepidopteran and coleopteran insect pests on crops depend on the expression of Bacillus thuringiensis insecticidal proteins, most of which permeabilize the membranes of gut epithelial cells of susceptible insects. However, insect control strategies involving a different mode of action would be valuable for managing the emergence of insect resistance. Toward this end, we demonstrate that ingestion of double-stranded (ds)RNAs supplied in an artificial diet triggers RNA interference in several coleopteran species, most notably the western corn rootworm (WCR) Diabrotica virgifera virgifera LeConte. This may result in larval stunting and mortality. Transgenic corn plants engineered to express WCR dsRNAs show a significant reduction in WCR feeding damage in a growth chamber assay, suggesting that the RNAi pathway can be exploited to control insect pests via in planta expression of a dsRNA.
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                Author and article information

                Journal
                101651677
                43556
                Nat Plants
                Nat Plants
                Nature plants
                2055-0278
                13 September 2016
                19 September 2016
                2016
                19 March 2017
                : 2
                : 16151
                Affiliations
                [1 ] Department of Plant Pathology and Microbiology, Center for Plant Cell Biology, Institute for Integrative Genome Biology, University of California, Riverside, CA 92521
                [3 ] Institute of Bioinformatics and Systems Biology, National Chiao Tung University, Hsin-Chu 300, Taiwan
                [4 ] Laboratory of Phytopathology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
                Author notes
                [* ] Correspondence to Hailing Jin. hailingj@ 123456ucr.edu
                [2]

                Current Address: Institute of Genetics, University of Munich Martinsried, Germany

                Article
                NIHMS814508
                10.1038/nplants.2016.151
                5040644
                27643635
                523e72ad-f9c7-4b1b-8863-44490c4c4888

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