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Tomato yellow leaf curl virus intergenic siRNAs target a host long noncoding RNA to modulate disease symptoms

Tomato yellow leaf curl virus (TYLCV) and its related begomoviruses cause fast-spreading diseases in tomato worldwide. How this virus induces diseases remains largely unclear. Here we report a noncoding RNA-mediated model to elucidate the molecular mechanisms of TYLCV-tomato interaction and disease...

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Autores principales: Yang, Yuwen, Liu, Tingli, Shen, Danyu, Wang, Jinyan, Ling, Xitie, Hu, Zhongze, Chen, Tianzi, Hu, Jieli, Huang, Junyu, Yu, Wengui, Dou, Daolong, Wang, Ming-Bo, Zhang, Baolong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6366713/
https://www.ncbi.nlm.nih.gov/pubmed/30668603
http://dx.doi.org/10.1371/journal.ppat.1007534
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author Yang, Yuwen
Liu, Tingli
Shen, Danyu
Wang, Jinyan
Ling, Xitie
Hu, Zhongze
Chen, Tianzi
Hu, Jieli
Huang, Junyu
Yu, Wengui
Dou, Daolong
Wang, Ming-Bo
Zhang, Baolong
author_facet Yang, Yuwen
Liu, Tingli
Shen, Danyu
Wang, Jinyan
Ling, Xitie
Hu, Zhongze
Chen, Tianzi
Hu, Jieli
Huang, Junyu
Yu, Wengui
Dou, Daolong
Wang, Ming-Bo
Zhang, Baolong
author_sort Yang, Yuwen
collection PubMed
description Tomato yellow leaf curl virus (TYLCV) and its related begomoviruses cause fast-spreading diseases in tomato worldwide. How this virus induces diseases remains largely unclear. Here we report a noncoding RNA-mediated model to elucidate the molecular mechanisms of TYLCV-tomato interaction and disease development. The circular ssDNA genome of TYLCV contains a noncoding intergenic region (IR), which is known to mediate viral DNA replication and transcription in host cells, but has not been reported to contribute directly to viral disease development. We demonstrate that the IR is transcribed in dual orientations during plant infection and confers abnormal phenotypes in tomato independently of protein-coding regions of the viral genome. We show that the IR sequence has a 25-nt segment that is almost perfectly complementary to a long noncoding RNA (lncRNA, designated as SlLNR1) in TYLCV-susceptible tomato cultivars but not in resistant cultivars which contains a 14-nt deletion in the 25-nt region. Consequently, we show that viral small-interfering RNAs (vsRNAs) derived from the 25-nt IR sequence induces silencing of SlLNR1 in susceptible tomato plants but not resistant plants, and this SlLNR1 downregulation is associated with stunted and curled leaf phenotypes reminiscent of TYLCV symptoms. These results suggest that the lncRNA interacts with the IR-derived vsRNAs to control disease development during TYLCV infection. Consistent with its possible function in virus disease development, over-expression of SlLNR1 in tomato reduces the accumulation of TYLCV. Furthermore, gene silencing of the SlLNR1 in the tomato plants induced TYLCV-like leaf phenotypes without viral infection. Our results uncover a previously unknown interaction between vsRNAs and host lncRNA, and provide a plausible model for TYLCV-induced diseases and host antiviral immunity, which would help to develop effective strategies for the control of this important viral pathogen.
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spelling pubmed-63667132019-02-22 Tomato yellow leaf curl virus intergenic siRNAs target a host long noncoding RNA to modulate disease symptoms Yang, Yuwen Liu, Tingli Shen, Danyu Wang, Jinyan Ling, Xitie Hu, Zhongze Chen, Tianzi Hu, Jieli Huang, Junyu Yu, Wengui Dou, Daolong Wang, Ming-Bo Zhang, Baolong PLoS Pathog Research Article Tomato yellow leaf curl virus (TYLCV) and its related begomoviruses cause fast-spreading diseases in tomato worldwide. How this virus induces diseases remains largely unclear. Here we report a noncoding RNA-mediated model to elucidate the molecular mechanisms of TYLCV-tomato interaction and disease development. The circular ssDNA genome of TYLCV contains a noncoding intergenic region (IR), which is known to mediate viral DNA replication and transcription in host cells, but has not been reported to contribute directly to viral disease development. We demonstrate that the IR is transcribed in dual orientations during plant infection and confers abnormal phenotypes in tomato independently of protein-coding regions of the viral genome. We show that the IR sequence has a 25-nt segment that is almost perfectly complementary to a long noncoding RNA (lncRNA, designated as SlLNR1) in TYLCV-susceptible tomato cultivars but not in resistant cultivars which contains a 14-nt deletion in the 25-nt region. Consequently, we show that viral small-interfering RNAs (vsRNAs) derived from the 25-nt IR sequence induces silencing of SlLNR1 in susceptible tomato plants but not resistant plants, and this SlLNR1 downregulation is associated with stunted and curled leaf phenotypes reminiscent of TYLCV symptoms. These results suggest that the lncRNA interacts with the IR-derived vsRNAs to control disease development during TYLCV infection. Consistent with its possible function in virus disease development, over-expression of SlLNR1 in tomato reduces the accumulation of TYLCV. Furthermore, gene silencing of the SlLNR1 in the tomato plants induced TYLCV-like leaf phenotypes without viral infection. Our results uncover a previously unknown interaction between vsRNAs and host lncRNA, and provide a plausible model for TYLCV-induced diseases and host antiviral immunity, which would help to develop effective strategies for the control of this important viral pathogen. Public Library of Science 2019-01-22 /pmc/articles/PMC6366713/ /pubmed/30668603 http://dx.doi.org/10.1371/journal.ppat.1007534 Text en © 2019 Yang et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Yang, Yuwen
Liu, Tingli
Shen, Danyu
Wang, Jinyan
Ling, Xitie
Hu, Zhongze
Chen, Tianzi
Hu, Jieli
Huang, Junyu
Yu, Wengui
Dou, Daolong
Wang, Ming-Bo
Zhang, Baolong
Tomato yellow leaf curl virus intergenic siRNAs target a host long noncoding RNA to modulate disease symptoms
title Tomato yellow leaf curl virus intergenic siRNAs target a host long noncoding RNA to modulate disease symptoms
title_full Tomato yellow leaf curl virus intergenic siRNAs target a host long noncoding RNA to modulate disease symptoms
title_fullStr Tomato yellow leaf curl virus intergenic siRNAs target a host long noncoding RNA to modulate disease symptoms
title_full_unstemmed Tomato yellow leaf curl virus intergenic siRNAs target a host long noncoding RNA to modulate disease symptoms
title_short Tomato yellow leaf curl virus intergenic siRNAs target a host long noncoding RNA to modulate disease symptoms
title_sort tomato yellow leaf curl virus intergenic sirnas target a host long noncoding rna to modulate disease symptoms
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6366713/
https://www.ncbi.nlm.nih.gov/pubmed/30668603
http://dx.doi.org/10.1371/journal.ppat.1007534
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