A combined microRNA and transcriptome analyses illuminates the resistance response of rice against brown planthopper

Abstract Background The brown planthopper (BPH, Nilaparvata lugens Stål) is a kind of phloem-feeding pest that adversely affects rice yield. Recently, the BPH-resistance gene, BPH6, was cloned and applied in rice breeding to effectively control BPH. However, the molecular mechanisms underlying BPH6...

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Main Authors: Jiaoyan Tan, Yan Wu, Jianping Guo, Huimin Li, Lili Zhu, Rongzhi Chen, Guangcun He, Bo Du
Format: Article
Language:English
Published: BMC 2020-02-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-020-6556-6
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spelling doaj-fde5e648f7224fd08ffce4ec96a3c5362021-02-14T12:22:26ZengBMCBMC Genomics1471-21642020-02-0121111710.1186/s12864-020-6556-6A combined microRNA and transcriptome analyses illuminates the resistance response of rice against brown planthopperJiaoyan Tan0Yan Wu1Jianping Guo2Huimin Li3Lili Zhu4Rongzhi Chen5Guangcun He6Bo Du7State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityAbstract Background The brown planthopper (BPH, Nilaparvata lugens Stål) is a kind of phloem-feeding pest that adversely affects rice yield. Recently, the BPH-resistance gene, BPH6, was cloned and applied in rice breeding to effectively control BPH. However, the molecular mechanisms underlying BPH6 are poorly understood. Results Here, an integrated miRNA and mRNA expression profiling analysis was performed on BPH6-transgenic (BPH6G) and Nipponbare (wild type, WT) plants after BPH infestation, and a total of 217 differentially expressed miRNAs (DEMs) and 7874 differentially expressed mRNAs (DEGs) were identified. 29 miRNAs, including members of miR160, miR166 and miR169 family were opposite expressed during early or late feeding stages between the two varieties, whilst 9 miRNAs were specifically expressed in BPH6G plants, suggesting involvement of these miRNAs in BPH6-mediated resistance to BPH. In the transcriptome analysis, 949 DEGs were opposite expressed during early or late feeding stages of the two genotypes, which were enriched in metabolic processes, cellular development, cell wall organization, cellular component movement and hormone transport, and certain primary and secondary metabolite synthesis. 24 genes were further selected as candidates for BPH resistance. Integrated analysis of the DEMs and DEGs showed that 34 miRNAs corresponding to 42 target genes were candidate miRNA-mRNA pairs for BPH resistance, 18 pairs were verified by qRT-PCR, and two pairs were confirmed by in vivo analysis. Conclusions For the first time, we reported integrated small RNA and transcriptome sequencing to illustrate resistance mechanisms against BPH in rice. Our results provide a valuable resource to ascertain changes in BPH-induced miRNA and mRNA expression profiles and enable to comprehend plant-insect interactions and find a way for efficient insect control.https://doi.org/10.1186/s12864-020-6556-6Brown planthopperBPH6Integrated analysismiRNA-mRNA interactionResistance mechanism
collection DOAJ
language English
format Article
sources DOAJ
author Jiaoyan Tan
Yan Wu
Jianping Guo
Huimin Li
Lili Zhu
Rongzhi Chen
Guangcun He
Bo Du
spellingShingle Jiaoyan Tan
Yan Wu
Jianping Guo
Huimin Li
Lili Zhu
Rongzhi Chen
Guangcun He
Bo Du
A combined microRNA and transcriptome analyses illuminates the resistance response of rice against brown planthopper
BMC Genomics
Brown planthopper
BPH6
Integrated analysis
miRNA-mRNA interaction
Resistance mechanism
author_facet Jiaoyan Tan
Yan Wu
Jianping Guo
Huimin Li
Lili Zhu
Rongzhi Chen
Guangcun He
Bo Du
author_sort Jiaoyan Tan
title A combined microRNA and transcriptome analyses illuminates the resistance response of rice against brown planthopper
title_short A combined microRNA and transcriptome analyses illuminates the resistance response of rice against brown planthopper
title_full A combined microRNA and transcriptome analyses illuminates the resistance response of rice against brown planthopper
title_fullStr A combined microRNA and transcriptome analyses illuminates the resistance response of rice against brown planthopper
title_full_unstemmed A combined microRNA and transcriptome analyses illuminates the resistance response of rice against brown planthopper
title_sort combined microrna and transcriptome analyses illuminates the resistance response of rice against brown planthopper
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2020-02-01
description Abstract Background The brown planthopper (BPH, Nilaparvata lugens Stål) is a kind of phloem-feeding pest that adversely affects rice yield. Recently, the BPH-resistance gene, BPH6, was cloned and applied in rice breeding to effectively control BPH. However, the molecular mechanisms underlying BPH6 are poorly understood. Results Here, an integrated miRNA and mRNA expression profiling analysis was performed on BPH6-transgenic (BPH6G) and Nipponbare (wild type, WT) plants after BPH infestation, and a total of 217 differentially expressed miRNAs (DEMs) and 7874 differentially expressed mRNAs (DEGs) were identified. 29 miRNAs, including members of miR160, miR166 and miR169 family were opposite expressed during early or late feeding stages between the two varieties, whilst 9 miRNAs were specifically expressed in BPH6G plants, suggesting involvement of these miRNAs in BPH6-mediated resistance to BPH. In the transcriptome analysis, 949 DEGs were opposite expressed during early or late feeding stages of the two genotypes, which were enriched in metabolic processes, cellular development, cell wall organization, cellular component movement and hormone transport, and certain primary and secondary metabolite synthesis. 24 genes were further selected as candidates for BPH resistance. Integrated analysis of the DEMs and DEGs showed that 34 miRNAs corresponding to 42 target genes were candidate miRNA-mRNA pairs for BPH resistance, 18 pairs were verified by qRT-PCR, and two pairs were confirmed by in vivo analysis. Conclusions For the first time, we reported integrated small RNA and transcriptome sequencing to illustrate resistance mechanisms against BPH in rice. Our results provide a valuable resource to ascertain changes in BPH-induced miRNA and mRNA expression profiles and enable to comprehend plant-insect interactions and find a way for efficient insect control.
topic Brown planthopper
BPH6
Integrated analysis
miRNA-mRNA interaction
Resistance mechanism
url https://doi.org/10.1186/s12864-020-6556-6
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