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      Plant miRNA Cross-Kingdom Transfer Targeting Parasitic and Mutualistic Organisms as a Tool to Advance Modern Agriculture

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          Abstract

          MicroRNAs (miRNAs), defined as small non-coding RNA molecules, are fine regulators of gene expression. In plants, miRNAs are well-known for regulating processes spanning from cell development to biotic and abiotic stress responses. Recently, miRNAs have been investigated for their potential transfer to distantly related organisms where they may exert regulatory functions in a cross-kingdom fashion. Cross-kingdom miRNA transfer has been observed in host-pathogen relations as well as symbiotic or mutualistic relations. All these can have important implications as plant miRNAs can be exploited to inhibit pathogen development or aid mutualistic relations. Similarly, miRNAs from eukaryotic organisms can be transferred to plants, thus suppressing host immunity. This two-way lane could have a significant impact on understanding inter-species relations and, more importantly, could leverage miRNA-based technologies for agricultural practices. Additionally, artificial miRNAs (amiRNAs) produced by engineered plants can be transferred to plant-feeding organisms in order to specifically regulate their cross-kingdom target genes. This minireview provides a brief overview of cross-kingdom plant miRNA transfer, focusing on parasitic and mutualistic relations that can have an impact on agricultural practices and discusses some opportunities related to miRNA-based technologies. Although promising, miRNA cross-kingdom transfer remains a debated argument. Several mechanistic aspects, such as the availability, transfer, and uptake of miRNAs, as well as their potential to alter gene expression in a cross-kingdom manner, remain to be addressed.

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          Most cited references49

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

          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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            Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen

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              Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene.

              Secreted parasitism proteins encoded by parasitism genes expressed in esophageal gland cells mediate infection and parasitism of plants by root-knot nematodes (RKN). Parasitism gene 16D10 encodes a conserved RKN secretory peptide that stimulates root growth and functions as a ligand for a putative plant transcription factor. We used in vitro and in vivo RNA interference approaches to silence this parasitism gene in RKN and validate that the parasitism gene has an essential function in RKN parasitism of plants. Ingestion of 16D10 dsRNA in vitro silenced the target parasitism gene in RKN and resulted in reduced nematode infectivity. In vivo expression of 16D10 dsRNA in Arabidopsis resulted in resistance effective against the four major RKN species. Because no known natural resistance gene has this wide effective range of RKN resistance, bioengineering crops expressing dsRNA that silence target RKN parasitism genes to disrupt the parasitic process represents a viable and flexible means of developing novel durable RKN-resistant crops and could provide crops with unprecedented broad resistance to RKN.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                23 June 2020
                2020
                : 11
                : 930
                Affiliations
                [1] 1Department of Biology and Biotechnology “L. Spallanzani”, University of Pavia , Pavia, Italy
                [2] 2Institute for Sustainable Plant Protection, National Council of Research, Research Unit of Bari , Bari, Italy
                Author notes

                Edited by: Jeremy Bruton Sweet, Sweet Environmental Consultants, Cambridge, UK

                Reviewed by: Rui Shi, North Carolina State University, United States; Karl-Heinz Kogel, University of Giessen, Germany

                *Correspondence: Anca Macovei, anca.macovei@ 123456unipv.it

                This article was submitted to Plant Biotechnology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2020.00930
                7325723
                32655608
                7de6424d-10fd-432e-bcdd-7a67374bb778
                Copyright © 2020 Gualtieri, Leonetti and Macovei

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 31 January 2020
                : 08 June 2020
                Page count
                Figures: 0, Tables: 2, Equations: 0, References: 58, Pages: 7, Words: 3386
                Categories
                Plant Science
                Mini Review

                Plant science & Botany
                agriculture,cross-kingdom,micrornas,mutualism,pathogen,plant
                Plant science & Botany
                agriculture, cross-kingdom, micrornas, mutualism, pathogen, plant

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