Combined miRNA and mRNA sequencing reveals the defensive strategies of resistant YHY15 rice against differentially virulent brown planthoppers

Bin Yu; Mengjia Geng; Yu Xue; Qingqing Yu; Bojie Lu; Miao Liu; Yuhan Shao; Chenxi Li; Jingang Xu; Jintao Li; Wei Hu; Hengmin Tang; Peng Li; Qingsong Liu; Shengli Jing

doi:10.3389/fpls.2024.1366515

Combined miRNA and mRNA sequencing reveals the defensive strategies of resistant YHY15 rice against differentially virulent brown planthoppers

Front Plant Sci. 2024 Mar 18:15:1366515. doi: 10.3389/fpls.2024.1366515. eCollection 2024.

Authors

Bin Yu¹, Mengjia Geng¹, Yu Xue¹, Qingqing Yu¹, Bojie Lu², Miao Liu¹, Yuhan Shao¹, Chenxi Li¹, Jingang Xu¹, Jintao Li¹, Wei Hu³, Hengmin Tang¹, Peng Li¹, Qingsong Liu^{1

4}, Shengli Jing¹

Affiliations

¹ College of Life Sciences, Xinyang Normal University, Xinyang, China.
² Hubei Provincial Key Laboratory for Protection and Application of Special Plant Germplasm in Wuling Area of China, College of Life Sciences, South-Central Minzu University, Wuhan, China.
³ Guangdong Provincial Key Laboratory of New Technology in Rice Breeding, Rice Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, China.
⁴ State Key Laboratory of Cotton Bio-breeding and Integrated Utilization, State Key Laboratory of Crop Stress Adaptation and Improvement, Key Laboratory of Plant Stress Biology, School of Life Sciences, Henan University, Kaifeng, China.

Abstract

Introduction: The brown planthopper (BPH) poses a significant threat to rice production in Asia. The use of resistant rice varieties has been effective in managing this pest. However, the adaptability of BPH to resistant rice varieties has led to the emergence of virulent populations, such as biotype Y BPH. YHY15 rice, which carries the BPH resistance gene Bph15, exhibits notable resistance to biotype 1 BPH but is susceptible to biotype Y BPH. Limited information exists regarding how resistant rice plants defend against BPH populations with varying levels of virulence.

Methods: In this study, we integrated miRNA and mRNA expression profiling analyses to study the differential responses of YHY15 rice to both avirulent (biotype 1) and virulent (biotype Y) BPH.

Results: YHY15 rice demonstrated a rapid response to biotype Y BPH infestation, with significant transcriptional changes occurring within 6 hours. The biotype Y-responsive genes were notably enriched in photosynthetic processes. Accordingly, biotype Y BPH infestation induced more intense transcriptional responses, affecting miRNA expression, defenserelated metabolic pathways, phytohormone signaling, and multiple transcription factors. Additionally, callose deposition was enhanced in biotype Y BPH-infested rice seedlings.

Discussion: These findings provide comprehensive insights into the defense mechanisms of resistant rice plants against virulent BPH, and may potentially guide the development of insect-resistant rice varieties.

Keywords: Bph15; brown planthopper; resistance mechanism; rice; virulent populations.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by grants from the National Natural Science Foundation of China (U1704111, 32372548 and 31401732), ZHONGYUAN YINGCAI JIHUA (ZYYCYU202012165), the Open Project Funding of the State Key Laboratory of Crop Stress Adaptation and Improvement (2023KF10), Young Elite Scientists Sponsorship Program by CAST (2023QNRC001), and the National Key Research and Development Program of China (2022YFD1401600).