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Systematic identification of miRNA-regulatory networks unveils their potential roles in sugarcane response to Sorghum mosaic virus infection
BACKGROUND: Sugarcane mosaic disease (SMD) is a major viral disease of sugarcane (Saccharum spp.) worldwide. Sorghum mosaic virus (SrMV) is the dominant pathogen of SMD in the sugarcane planting areas of China. There is no report on miRNAs and their regulatory networks in sugarcane response to SrMV...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9118776/ https://www.ncbi.nlm.nih.gov/pubmed/35585486 http://dx.doi.org/10.1186/s12870-022-03641-6 |
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author | Su, Yachun Peng, Qiong Ling, Hui You, Chuihuai Wu, Qibin Xu, Liping Que, Youxiong |
author_facet | Su, Yachun Peng, Qiong Ling, Hui You, Chuihuai Wu, Qibin Xu, Liping Que, Youxiong |
author_sort | Su, Yachun |
collection | PubMed |
description | BACKGROUND: Sugarcane mosaic disease (SMD) is a major viral disease of sugarcane (Saccharum spp.) worldwide. Sorghum mosaic virus (SrMV) is the dominant pathogen of SMD in the sugarcane planting areas of China. There is no report on miRNAs and their regulatory networks in sugarcane response to SrMV infection. RESULTS: In this study, small RNA sequencing (sRNA-seq) of samples from the leaves of SMD-susceptible variety ROC22 and -resistant variety FN39 infected by SrMV was performed. A total of 132 mature miRNAs (55 known miRNAs and 77 novel miRNAs) corresponding to 1,037 target genes were identified. After the SrMV attack, there were 30 differentially expressed miRNAs (17 up-regulated and 13 down-regulated) in FN39 and 19 in ROC22 (16 up-regulated and 3 down-regulated). Besides, there were 18 and 7 variety-specific differentially expressed miRNAs for FN39 and ROC22, respectively. KEGG enrichment analysis showed that the differentially expressed miRNAs targeted genes involved in several disease resistance-related pathways, such as mRNA surveillance, plant pathway interaction, sulfur metabolism, and regulation of autophagy. The reliability of sequencing data, and the expression patterns / regulation relationships between the selected differentially expressed miRNAs and their target genes in ROC22 and FN39 were confirmed by quantitative real-time PCR. A regulatory network diagram of differentially expressed miRNAs and their predicted target genes in sugarcane response to SrMV infection was sketched. In addition, precursor sequences of three candidate differentially expressed novel miRNAs (nov_3741, nov_22650 and nov_40875) were cloned from the ROC22 leaf infected by SrMV. Transient overexpression demonstrated that they could induce the accumulation of hydrogen peroxide and the expression level of hypersensitive response marker genes, salicylic acid-responsive genes and ethylene synthesis-depended genes in Nicotiana benthamiana. It is thus speculated that these three miRNAs may be involved in regulating the early immune response of sugarcane plants following SrMV infection. CONCLUSIONS: This study lays a foundation for revealing the miRNA regulation mechanism in the interaction of sugarcane and SrMV, and also provides a resource for miRNAs and their predicted target genes for SrMV resistance improvement in sugarcane. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03641-6. |
format | Online Article Text |
id | pubmed-9118776 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-91187762022-05-20 Systematic identification of miRNA-regulatory networks unveils their potential roles in sugarcane response to Sorghum mosaic virus infection Su, Yachun Peng, Qiong Ling, Hui You, Chuihuai Wu, Qibin Xu, Liping Que, Youxiong BMC Plant Biol Research BACKGROUND: Sugarcane mosaic disease (SMD) is a major viral disease of sugarcane (Saccharum spp.) worldwide. Sorghum mosaic virus (SrMV) is the dominant pathogen of SMD in the sugarcane planting areas of China. There is no report on miRNAs and their regulatory networks in sugarcane response to SrMV infection. RESULTS: In this study, small RNA sequencing (sRNA-seq) of samples from the leaves of SMD-susceptible variety ROC22 and -resistant variety FN39 infected by SrMV was performed. A total of 132 mature miRNAs (55 known miRNAs and 77 novel miRNAs) corresponding to 1,037 target genes were identified. After the SrMV attack, there were 30 differentially expressed miRNAs (17 up-regulated and 13 down-regulated) in FN39 and 19 in ROC22 (16 up-regulated and 3 down-regulated). Besides, there were 18 and 7 variety-specific differentially expressed miRNAs for FN39 and ROC22, respectively. KEGG enrichment analysis showed that the differentially expressed miRNAs targeted genes involved in several disease resistance-related pathways, such as mRNA surveillance, plant pathway interaction, sulfur metabolism, and regulation of autophagy. The reliability of sequencing data, and the expression patterns / regulation relationships between the selected differentially expressed miRNAs and their target genes in ROC22 and FN39 were confirmed by quantitative real-time PCR. A regulatory network diagram of differentially expressed miRNAs and their predicted target genes in sugarcane response to SrMV infection was sketched. In addition, precursor sequences of three candidate differentially expressed novel miRNAs (nov_3741, nov_22650 and nov_40875) were cloned from the ROC22 leaf infected by SrMV. Transient overexpression demonstrated that they could induce the accumulation of hydrogen peroxide and the expression level of hypersensitive response marker genes, salicylic acid-responsive genes and ethylene synthesis-depended genes in Nicotiana benthamiana. It is thus speculated that these three miRNAs may be involved in regulating the early immune response of sugarcane plants following SrMV infection. CONCLUSIONS: This study lays a foundation for revealing the miRNA regulation mechanism in the interaction of sugarcane and SrMV, and also provides a resource for miRNAs and their predicted target genes for SrMV resistance improvement in sugarcane. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03641-6. BioMed Central 2022-05-19 /pmc/articles/PMC9118776/ /pubmed/35585486 http://dx.doi.org/10.1186/s12870-022-03641-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Su, Yachun Peng, Qiong Ling, Hui You, Chuihuai Wu, Qibin Xu, Liping Que, Youxiong Systematic identification of miRNA-regulatory networks unveils their potential roles in sugarcane response to Sorghum mosaic virus infection |
title | Systematic identification of miRNA-regulatory networks unveils their potential roles in sugarcane response to Sorghum mosaic virus infection |
title_full | Systematic identification of miRNA-regulatory networks unveils their potential roles in sugarcane response to Sorghum mosaic virus infection |
title_fullStr | Systematic identification of miRNA-regulatory networks unveils their potential roles in sugarcane response to Sorghum mosaic virus infection |
title_full_unstemmed | Systematic identification of miRNA-regulatory networks unveils their potential roles in sugarcane response to Sorghum mosaic virus infection |
title_short | Systematic identification of miRNA-regulatory networks unveils their potential roles in sugarcane response to Sorghum mosaic virus infection |
title_sort | systematic identification of mirna-regulatory networks unveils their potential roles in sugarcane response to sorghum mosaic virus infection |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9118776/ https://www.ncbi.nlm.nih.gov/pubmed/35585486 http://dx.doi.org/10.1186/s12870-022-03641-6 |
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