Transcriptional landscape of pathogen‐responsive lncRNAs in tomato unveils the role of hydrolase encoding genes in response to Botrytis cinerea invasion

• Published in: Plant, cell and environment Vol. 47; no. 2; pp. 651 - 663
• Main Authors: Chen, Daoguo, Zhang, Zhanquan, Chen, Yong, Li, Boqiang, Chen, Tong, Tian, Shiping
• Format: Journal Article
• Language: English
• Published: United States Wiley Subscription Services, Inc 01.02.2024
• Subjects: Botrytis - physiology; Botrytis cinerea; Carboxylesterase; Chitinase; defence response; Disease Resistance - genetics; Enzymatic activity; fruit; Fruits; fungal pathogen; Gene expression; Gene Expression Regulation, Plant; Gene silencing; Genes; Hydrolase; Hydrolases - metabolism; long noncoding RNA; Non-coding RNA; Pathogens; Plant Diseases - genetics; Plant Proteins - genetics; Plant Proteins - metabolism; RNA, Long Noncoding - genetics; Solanum lycopersicum - genetics; Tomatoes; long noncoding RNA; defence response; fungal pathogen; fruit
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.14757

LncRNAs have gained increasing attention owing to their important regulatory roles on growth and stress responses of plants. However, the mechanisms underlying the functions of lncRNAs in fruit‐pathogen interaction are still largely unknown. In this study, a total of 273 lncRNAs responding to Botrytis cinerea infection were identified in tomato fruit, among which a higher percentage of antisense lncRNAs were targeted to the genes enriched in hydrolase activity. To ascertain the roles of these lncRNAs, seven hydrolase‐related transcripts were transiently knocked‐down by virus‐induced gene silencing. Silencing of lncRNACXE20 reduced the expression level of a carboxylesterase gene, further enhancing the resistance of tomato to B. cinerea. In contrast, silencing of lncRNACHI, lncRNAMMP, lncRNASBT1.9 and lncRNAPME1.9 impaired the resistance to B. cinerea, respectively. Further RT‐qPCR assay and enzymatic activity detection displayed that the attenuated resistance of lncRNAMMP and lncRNASBT1.9‐silenced plants was associated with the inhibition on the expression of JA‐related genes, while the decreased resistance of lncRNACHI‐silenced plants resulted in reduced chitinase activity. Collectively, these results may provide references for deciphering the mechanisms underlying specific lncRNAs to interfere with B. cinerea infection by regulating the expression of defence‐related genes or affecting hydrolase activity. Summary Statement To add more references to the mechanisms underlying the interaction between fruit—Botrytis cinerea interaction, the lncRNAs induced by B. cinerea in tomato fruit were identified and their roles were preliminarily investigated. The results revealed that specific lncRNAs are involved in fruit—B. cinerea interaction by regulating the expression of defence‐related genes or affecting hydrolase activity.