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      Tomato lncRNA23468 functions as a competing endogenous RNA to modulate NBS-LRR genes by decoying miR482b in the tomato -Phytophthora infestans interaction

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          Abstract

          Our previous studies indicated that tomato miR482b could negatively regulate the resistance of tomato to Phytophthora infestans and the expression of miR482b was decreased after inoculation with P. infestans. However, the mechanism by which the accumulation of miR482b is suppressed remains unclear. In this study, we wrote a program to identify 89 long noncoding RNA (lncRNA)-originated endogenous target mimics (eTMs) for 46 miRNAs from our RNA-Seq data. Three tomato lncRNAs, lncRNA23468, lncRNA01308 and lncRNA13262, contained conserved eTM sites for miR482b. When lncRNA23468 was overexpressed in tomato, miR482b expression was significantly decreased, and the expression of the target genes, NBS-LRRs, was significantly increased, resulting in enhanced resistance to P. infestans. Silencing lncRNA23468 in tomato led to the increased accumulation of miR482b and decreased accumulation of NBS-LRRs, as well as reduced resistance to P. infestans. In addition, the accumulation of both miR482b and NBS-LRRs was not significantly changed in tomato plants that overexpressed lncRNA23468 with a mutated eTM site. Based on the VIGS system, a target gene of miR482b, Solyc02g036270.2, was silenced. The disease symptoms of the VIGS- Solyc02g036270.2 tomato plants were in accordance with those of tomato plants in which lncRNA23468 was silenced after inoculation with P. infestans. More severe disease symptoms were found in the modified plants than in the control plants. Our results demonstrate that lncRNAs functioning as eTMs may modulate the effects of miRNAs in tomato and provide insight into how the lncRNA23468-miR482b-NBS-LRR module regulates tomato resistance to P. infestans.

          A barrier against blight

          The interplay between various non-protein-coding RNA molecules plays a critical role in managing tomato plants’ defenses against infection. Long non-coding RNA (lncRNA) molecules can modulate gene function by binding to other, complementary RNA molecules. Researchers led by Jun Meng and Yushi Luan at the Dalian University of Technology recently set out to identify lncRNAs that contribute to tomato resistance to the pathogen that causes late blight. Their team specifically sought lncRNAs targeting another RNA molecule known as miR482b, which they had previously found to weaken plant resistance to infection. They found that one such molecule, lncRNA23468, can counter the effects of miR482b and protect tomatoes against late blight by boosting the activity of genes involved in the immune response. These results thus offer important insights into the mechanisms underlying disease resistance in this important crop.

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          Most cited references 49

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          Virus-induced gene silencing in tomato.

          We have previously demonstrated that a tobacco rattle virus (TRV)-based vector can be used in virus-induced gene silencing (VIGS) to study gene function in Nicotiana benthamiana. Here we show that recombinant TRV infects tomato plants and induces efficient gene silencing. Using this system, we suppressed the PDS, CTR1 and CTR2 genes in tomato. Suppression of CTR1 led to a constitutive ethylene response phenotype and up-regulation of an ethylene response gene, CHITINASE B. This phenotype is similar to Arabidopsis ctr1 mutant plants. We have constructed a modified TRV vector based on the GATEWAY recombination system, allowing restriction- and ligation-free cloning. Our results show that tomato expressed sequence tags (ESTs) can easily be cloned into this modified vector using a single set of primers. Using this vector, we have silenced RbcS and an endogenous gene homologous to the tomato EST cLED3L14. In the future, this modified vector system will facilitate large-scale functional analysis of tomato ESTs.
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            Targeted 3' processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing.

            Noncoding RNA is emerging as an important regulator of gene expression in many organisms. We are characterizing RNA-mediated chromatin silencing of the Arabidopsis major floral repressor gene, FLC. Through suppressor mutagenesis, we identify a requirement for CstF64 and CstF77, two conserved RNA 3'-end-processing factors, in FLC silencing. However, FLC sense transcript 3' processing is not affected in the mutants. Instead, CstF64 and CstF77 are required for 3' processing of FLC antisense transcripts. A specific RNA-binding protein directs their activity to a proximal antisense polyadenylation site. This targeted processing triggers localized histone demethylase activity and results in reduced FLC sense transcription. Targeted 3' processing of antisense transcripts may be a common mechanism triggering transcriptional silencing of the corresponding sense gene.
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              Oomycete pathogens encode RNA silencing suppressors.

              Effectors are essential virulence proteins produced by a broad range of parasites, including viruses, bacteria, fungi, oomycetes, protozoa, insects and nematodes. Upon entry into host cells, pathogen effectors manipulate specific physiological processes or signaling pathways to subvert host immunity. Most effectors, especially those of eukaryotic pathogens, remain functionally uncharacterized. Here, we show that two effectors from the oomycete plant pathogen Phytophthora sojae suppress RNA silencing in plants by inhibiting the biogenesis of small RNAs. Ectopic expression of these Phytophthora suppressors of RNA silencing enhances plant susceptibility to both a virus and Phytophthora, showing that some eukaryotic pathogens have evolved virulence proteins that target host RNA silencing processes to promote infection. These findings identify RNA silencing suppression as a common strategy used by pathogens across kingdoms to cause disease and are consistent with RNA silencing having key roles in host defense.
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                Author and article information

                Contributors
                mengjun@dlut.edu.cn
                ysluan@dlut.edu.cn
                Journal
                Hortic Res
                Hortic Res
                Horticulture Research
                Nature Publishing Group UK (London )
                2052-7276
                1 February 2019
                1 February 2019
                2019
                : 6
                Affiliations
                [1 ]ISNI 0000 0000 9247 7930, GRID grid.30055.33, School of Life Science and Biotechnology, , Dalian University of Technology, ; 116024 Dalian, China
                [2 ]ISNI 0000 0000 9247 7930, GRID grid.30055.33, School of Computer Science and Technology, , Dalian University of Technology, ; 116024 Dalian, China
                Article
                96
                10.1038/s41438-018-0096-0
                6355781
                391fc55d-8229-4b98-963a-1122d70de5fe
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001809, National Natural Science Foundation of China (National Science Foundation of China);
                Award ID: 31471880
                Award ID: 61472061
                Award Recipient :
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                © The Author(s) 2019

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