Abstract

Summary Fungal diseases such as anthracnose substantially affect the growth of tea ( Camellia sinensis ) plants. Identifying resistance genes and elucidating the mechanisms of resistance is crucial for breeding anthracnose-resistant tea varieties. Small RNA transcriptome sequencing was used to analyze differentially expressed microRNAs (miRNAs) and their target genes in tea leaves at 6 d post-inoculation with Colletotrichum camelliae , combined with functional enrichment analysis. A novel regulatory axis was delineated – comprising long noncoding RNA Cslnc924 , CsmiR390a , CsTAS3 ( trans -acting siRNA), CsARF2s (auxin response factors), and CsOPR2 (12-oxo-phytodienoic acid reductase) – that plays a novel role for this axis in anthracnose resistance in tea plants. Mechanistically, the 257–511 bp region of Cslnc924 binds to the promoter region (−825 to −1053 bp) of CsmiR390a , thereby activating its transcription. This upregulation of CsmiR390a positively modulated the CsmiR390a-CsTAS3-CsARF2 module, leading to the reduced expression of ARF2s ( ARF2.1 and ARF2.2 ). Consequently, the suppression of CsOPR2-1 by ARF2s was alleviated, thereby enhancing anthracnose resistance in tea plants. This study reveals the regulatory role of the CsmiR390a–CsTAS3–CsARF2s module in tea–anthracnose resistance and deepens the understanding of lncRNA–miRNA–mRNA regulatory mechanisms in tea plant defense against fungal pathogens.