Journal of Integrative Agriculture ›› 2026, Vol. 25 ›› Issue (7): 2878-2889.DOI: 10.1016/j.jia.2025.03.026

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玉米小斑病菌circRNA与寄主miRNA互作对玉米防御反应的抑制作用

  

  • 收稿日期:2024-11-03 修回日期:2025-03-27 接受日期:2025-03-02 出版日期:2026-07-20 发布日期:2026-06-09

Pathogenic exonic circRNA from Cochliobolus heterostrophus interacts with host miRNA to suppress maize defense

Shaoqing Wang1,2* Meng Wang1,2*, Xinhua Wang1, 2, Jie Chen1, 2#   

  1. 1 School of Agriculture and Biology, Shanghai Jiaotong University, Shanghai 200240, China

    2 State Key Laboratory of Microbial Metabolism, Shanghai Jiaotong University, Shanghai 200240, China

  • Received:2024-11-03 Revised:2025-03-27 Accepted:2025-03-02 Online:2026-07-20 Published:2026-06-09
  • About author:#Correspondence Jie Chen, E-mail: jiechen59@sjtu.edu.cn * These authors contributed equally to this study.
  • Supported by:
    The project was supported by the National Key Research and Development Program of China (2023YFD1401500), the Special Cooperation Project of Inner Mongolia Autonomous Region and Shanghai Jiao Tong University, China (KJXM2023-12-01), the Key Project of Bayannur National Agricultural High-tech Industry Demonstration Zone, China (NMKJXM202209), and the China Agriculture Research System of MOF and MARA (CARS-02).

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摘要：

环状RNA（circRNA）是一类在不同生物中广泛存在的非编码RNA，但其生物学功能大多尚未明确，特别是其在植物与微生物互作中的作用研究较少。在本研究中，我们从玉米小斑病菌（Cochliobolus heterostrophus，简称C. heterostrophus）中鉴定出一种外显子来源的环状RNA（Che-circR2410），并且通过构建Che-circR2410和其前体基因（ChCYP51）的敲除和回补突变体并回接玉米叶片，调查其致病作用的变化。结果证明：Che-circR2410与其前体基因ChCYP51均参与调控C. heterostrophus对玉米叶片的致病性。进一步通过Che-circR2410的原位杂交实验和双荧光素酶报告系统分析，发现Che-circR2410定位在侵染的菌丝周边，可跨界与寄主细胞中的靶标zma-miR399e-5p相互作用。此外，构建了玉米 zma-miR399e 的瞬时沉默株，比较接种小斑病菌 Che-circR2410 的敲除突变株和野生株后造成的病斑面积，我们发现由野生型C. heterostrophus和Che-circR2410敲除突变株（∆ChcircR2410）在玉米zma-miR399e沉默突变体上引起的病斑面积无显著差异，进一步证明了Che-circR2410与zma-miR399e-5p在叶片内存在相互作用。此外，发现小斑病菌侵染玉米zma-miR399e 沉默株叶片形成的病斑面积均显著高于玉米野生株上的病斑面积，表明zma-miR399e参与调控玉米对小斑病菌的防御反应。进一步检测zma-miR399e预测的靶标基因在病菌侵染过程中的表达量，发现zma-miR399e能够参与调控自噬相关基因的表达，进而影响玉米防御反应。综上所述，本研究揭示了小斑病菌致病性外显子环状RNA 与其前体基因协同调控病菌致病性，且病菌环状RNA与寄主miRNA之间通过跨界互作调节病菌对玉米叶片的侵染。这一发现拓展了人们关于非编码RNA在C. heterostrophus与玉米互作中作用的认识。

Abstract:

Circular RNAs (circRNAs) are a group of widely discovered non-coding RNAs in different organisms, but their biological functions are largely unknown, especially in plant–microbial interactions.  In this study, we identified an exonic circRNA (Che-circR2410) from the fungus Cochliobolus heterostrophus that, together with its corresponding linear RNA ChCYP51, synergistically regulates the virulence of C. heterostrophus to maize.  Further in situ hybridization and dual-luciferase reporter assays revealed the interaction between pathogenic circRNA Che-circR2410 and its cross-kingdom host target, zma-miR399e-5p.  Additionally, lesion areas caused by both the wild type C. heterostrophus and the circR2410 knock-out strain (ΔChcircR2410) showed no significant difference on the maize miR399e silencing mutant, providing support for the interaction between Che-circR2410 and zma-miR399e-5p.  Moreover, we found that zma-miR399e affects the expression of autophagy-related genes, regulating maize immunity.  Thus, our findings reveal a cross–kingdom interaction between the pathogenic exonic circRNA and host miRNA, modulating C. heterostrophus infection in maize.  This study broadens our understanding of the C. heterostrophus-maize interaction at the level of non-coding RNA.

Key words: Cochliobolus heterostrophus , circRNA , cross–kingdom interaction ,  maize miRNA