Defense Regulatory Network Associated with circRNA in Rice in Response to Brown Planthopper Infestation

The brown planthopper (BPH), <i>Nilaparvata lugens</i> (Stål), a rice-specific pest, has risen to the top of the list of significant pathogens and insects in recent years. Host plant-mediated resistance is an efficient strategy for BPH control. Nonetheless, BPH resistance in rice cultiva...

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Main Authors: Hou-Hong Yang, Ya-Xuan Wang, Jing Xiao, Yi-Fan Jia, Fang Liu, Wei-Xia Wang, Qi Wei, Feng-Xiang Lai, Qiang Fu, Pin-Jun Wan
Format: Article
Language:English
Published: MDPI AG 2024-01-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/13/3/373
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author Hou-Hong Yang
Ya-Xuan Wang
Jing Xiao
Yi-Fan Jia
Fang Liu
Wei-Xia Wang
Qi Wei
Feng-Xiang Lai
Qiang Fu
Pin-Jun Wan
author_facet Hou-Hong Yang
Ya-Xuan Wang
Jing Xiao
Yi-Fan Jia
Fang Liu
Wei-Xia Wang
Qi Wei
Feng-Xiang Lai
Qiang Fu
Pin-Jun Wan
author_sort Hou-Hong Yang
collection DOAJ
description The brown planthopper (BPH), <i>Nilaparvata lugens</i> (Stål), a rice-specific pest, has risen to the top of the list of significant pathogens and insects in recent years. Host plant-mediated resistance is an efficient strategy for BPH control. Nonetheless, BPH resistance in rice cultivars has succumbed to the emergence of distinct virulent BPH populations. Circular RNAs (circRNAs) play a pivotal role in regulating plant–environment interactions; however, the mechanisms underlying their insect-resistant functions remain largely unexplored. In this study, we conducted an extensive genome-wide analysis using high-throughput sequencing to explore the response of rice circRNAs to BPH infestations. We identified a total of 186 circRNAs in IR56 rice across two distinct virulence groups: IR-IR56-BPH (referring to IR rice infested by IR56-BPH) and IR-TN1-BPH, along with a control group (IR-CK) without BPH infestation. Among them, 39 circRNAs were upregulated, and 43 circRNAs were downregulated in the comparison between IR-IR56-BPH and IR-CK. Furthermore, in comparison with IR-CK, 42 circRNAs exhibited upregulation in IR-TN1-BPH, while 42 circRNAs showed downregulation. The Gene Ontology and Kyoto Encyclopedia of Genes and Genomes enrichment analysis revealed that the targets of differentially expressed circRNAs were considerably enriched in a multitude of biological processes closely linked to the response to BPH infestations. Furthermore, we assessed a total of 20 randomly selected circRNAs along with their corresponding expression levels. Moreover, we validated the regulatory impact of circRNAs on miRNAs and mRNAs. These findings have led us to construct a conceptual model that circRNA is associated with the defense regulatory network in rice, which is likely facilitated by the mediation of their parental genes and competing endogenous RNA (ceRNA) networks. This model contributes to the understanding of several extensively studied processes in rice-BPH interactions.
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spelling doaj.art-b30eea4c17de46d1a55a08eeebe3f2742024-02-09T15:20:14ZengMDPI AGPlants2223-77472024-01-0113337310.3390/plants13030373Defense Regulatory Network Associated with circRNA in Rice in Response to Brown Planthopper InfestationHou-Hong Yang0Ya-Xuan Wang1Jing Xiao2Yi-Fan Jia3Fang Liu4Wei-Xia Wang5Qi Wei6Feng-Xiang Lai7Qiang Fu8Pin-Jun Wan9State Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou 311400, ChinaState Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou 311400, ChinaState Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou 311400, ChinaState Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou 311400, ChinaState Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou 311400, ChinaState Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou 311400, ChinaState Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou 311400, ChinaState Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou 311400, ChinaState Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou 311400, ChinaState Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou 311400, ChinaThe brown planthopper (BPH), <i>Nilaparvata lugens</i> (Stål), a rice-specific pest, has risen to the top of the list of significant pathogens and insects in recent years. Host plant-mediated resistance is an efficient strategy for BPH control. Nonetheless, BPH resistance in rice cultivars has succumbed to the emergence of distinct virulent BPH populations. Circular RNAs (circRNAs) play a pivotal role in regulating plant–environment interactions; however, the mechanisms underlying their insect-resistant functions remain largely unexplored. In this study, we conducted an extensive genome-wide analysis using high-throughput sequencing to explore the response of rice circRNAs to BPH infestations. We identified a total of 186 circRNAs in IR56 rice across two distinct virulence groups: IR-IR56-BPH (referring to IR rice infested by IR56-BPH) and IR-TN1-BPH, along with a control group (IR-CK) without BPH infestation. Among them, 39 circRNAs were upregulated, and 43 circRNAs were downregulated in the comparison between IR-IR56-BPH and IR-CK. Furthermore, in comparison with IR-CK, 42 circRNAs exhibited upregulation in IR-TN1-BPH, while 42 circRNAs showed downregulation. The Gene Ontology and Kyoto Encyclopedia of Genes and Genomes enrichment analysis revealed that the targets of differentially expressed circRNAs were considerably enriched in a multitude of biological processes closely linked to the response to BPH infestations. Furthermore, we assessed a total of 20 randomly selected circRNAs along with their corresponding expression levels. Moreover, we validated the regulatory impact of circRNAs on miRNAs and mRNAs. These findings have led us to construct a conceptual model that circRNA is associated with the defense regulatory network in rice, which is likely facilitated by the mediation of their parental genes and competing endogenous RNA (ceRNA) networks. This model contributes to the understanding of several extensively studied processes in rice-BPH interactions.https://www.mdpi.com/2223-7747/13/3/373circular RNAs (circRNAs)<i>Nilaparvata lugens</i>IR56 ricerice-BPH interaction
spellingShingle Hou-Hong Yang
Ya-Xuan Wang
Jing Xiao
Yi-Fan Jia
Fang Liu
Wei-Xia Wang
Qi Wei
Feng-Xiang Lai
Qiang Fu
Pin-Jun Wan
Defense Regulatory Network Associated with circRNA in Rice in Response to Brown Planthopper Infestation
Plants
circular RNAs (circRNAs)
<i>Nilaparvata lugens</i>
IR56 rice
rice-BPH interaction
title Defense Regulatory Network Associated with circRNA in Rice in Response to Brown Planthopper Infestation
title_full Defense Regulatory Network Associated with circRNA in Rice in Response to Brown Planthopper Infestation
title_fullStr Defense Regulatory Network Associated with circRNA in Rice in Response to Brown Planthopper Infestation
title_full_unstemmed Defense Regulatory Network Associated with circRNA in Rice in Response to Brown Planthopper Infestation
title_short Defense Regulatory Network Associated with circRNA in Rice in Response to Brown Planthopper Infestation
title_sort defense regulatory network associated with circrna in rice in response to brown planthopper infestation
topic circular RNAs (circRNAs)
<i>Nilaparvata lugens</i>
IR56 rice
rice-BPH interaction
url https://www.mdpi.com/2223-7747/13/3/373
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