MicroRNAs involved in the trans-kingdom gene regulation in the interaction of maize kernels and Fusarium verticillioides

Qing Qu; Ning Liu; Qianfu Su; Xinfang Liu; Hui Jia; Yuwei Liu; Manli Sun; Zhiyan Cao; Jingao Dong

doi:10.1016/j.ijbiomac.2023.125046

MicroRNAs involved in the trans-kingdom gene regulation in the interaction of maize kernels and Fusarium verticillioides

Int J Biol Macromol. 2023 Jul 1;242(Pt 4):125046. doi: 10.1016/j.ijbiomac.2023.125046. Epub 2023 May 26.

Authors

Qing Qu¹, Ning Liu¹, Qianfu Su², Xinfang Liu³, Hui Jia¹, Yuwei Liu⁴, Manli Sun¹, Zhiyan Cao⁵, Jingao Dong⁶

Affiliations

¹ Plant Pathogenic Mycotoxin and Molecular Plant Pathology Laboratory, Hebei Key Laboratory of Plant Physiology and Molecular Pathology, Hebei Agriculture University, Baoding 071001, China; State Key Laboratory of North China Crop Improvement and Regulation, Hebei Agriculture University, Baoding 071001, China.
² Jilin Academy of Agricultural Sciences, Jilin 130033, China.
³ Corn Research Institute, Liaoning Academy of Agricultural Sciences, Shenyang 110161, China.
⁴ Plant Pathogenic Mycotoxin and Molecular Plant Pathology Laboratory, Hebei Key Laboratory of Plant Physiology and Molecular Pathology, Hebei Agriculture University, Baoding 071001, China.
⁵ Plant Pathogenic Mycotoxin and Molecular Plant Pathology Laboratory, Hebei Key Laboratory of Plant Physiology and Molecular Pathology, Hebei Agriculture University, Baoding 071001, China; State Key Laboratory of North China Crop Improvement and Regulation, Hebei Agriculture University, Baoding 071001, China. Electronic address: caoyan208@126.com.
⁶ Plant Pathogenic Mycotoxin and Molecular Plant Pathology Laboratory, Hebei Key Laboratory of Plant Physiology and Molecular Pathology, Hebei Agriculture University, Baoding 071001, China; State Key Laboratory of North China Crop Improvement and Regulation, Hebei Agriculture University, Baoding 071001, China. Electronic address: dongjingao@126.com.

PMID: 37245767
DOI: 10.1016/j.ijbiomac.2023.125046

Abstract

Maize ear rot is a widespread disease and the main pathogen is Fusarium verticillioides. Plant microRNAs (miRNAs) have great effects on disease resistance and it has been reported that maize miRNA participates in defense responses in maize ear rot. However, the trans-kingdom regulation of miRNAs between maize and F. verticillioides remains uncharacterized. In this study, the relationship between miRNA-like RNAs (milRNAs) of F. verticillioides and pathogenicity was investigated, followed by sRNA analysis and degradome sequencing of miRNA profiles and the target genes of maize and F. verticillioides after inoculation. It was found that the milRNA biogenesis positively regulated the pathogenicity of F. verticillioides by knocking out the gene FvDicer2-encoded Dicer-like protein in F. verticillioides. Following inoculation with F. verticillioides, 284 known and 6571 novel miRNAs were obtained in maize, including 28 miRNAs differentially expressed at multiple time points. The target genes of maize differentially expressed miRNAs in F. verticillioides mediated multiple pathways, including autophagy and MAPK signaling pathway. Fifty-one novel F. verticillioides milRNAs were predicted to target 333 genes in maize involved in MAPK signaling pathways, plant hormone signaling transduction and plant-pathogen interaction pathways. Additionally, the miR528b-5p in maize targeted the mRNA of FvTTP which encoded a twice transmembrane protein in F. verticillioides. The FvTTP-knockout mutants displayed decreased pathogenicity and reduced synthesis of fumonisins. Thus, by interfering with the translation of FvTTP, the miR528b-5p inhibited F. verticillioides infection. These findings suggested a novel function of miR528 in resisting F. verticillioides infection. The miRNAs identified in this research and their putative target genes can be used to further elucidate the trans-kingdom functions of microRNAs in plant pathogen interaction.

Keywords: Fusarium verticillioides; Maize ear rot; MicroRNA; Trans-kingdom; miR528.

MeSH terms

Disease Resistance / genetics
Fumonisins* / metabolism
Fusarium* / metabolism
MicroRNAs* / genetics
MicroRNAs* / metabolism
Plant Diseases / genetics
Zea mays / genetics
Zea mays / metabolism

Substances

MicroRNAs
Fumonisins

Supplementary concepts

Fusarium verticillioides