The lncRNA39896–miR166b–HDZs module affects tomato resistance to Phytophthora infestans

• Published in: Journal of integrative plant biology Vol. 64; no. 10; pp. 1979 - 1993
• Main Authors: Hong, Yuhui, Zhang, Yuanyuan, Cui, Jun, Meng, Jun, Chen, Yinhua, Zhang, Chengwei, Yang, Jinxiao, Luan, Yushi
• Format: Journal Article
• Language: English
• Published: Hoboken Wiley Subscription Services, Inc 01.10.2022; State Key Laboratory of Rice Biology,China National Rice Research Institute,Hangzhou 311400,China%School of Bioengineering,Dalian University of Technology,Dalian 116024,China; School of Bioengineering,Dalian University of Technology,Dalian 116024,China%School of Bioengineering,Dalian University of Technology,Dalian 116024,China; College of Life Science,Hunan Normal University,Changsha 410081,China%School of Computer Science and Technology,Dalian University of Technology,Dalian 116024,China%Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresource,College of Tropical Crops,Hainan University,Haikou 570228,China%Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding,Beijing Academy of Agriculture&Forestry Sciences,Beijing 100000,China
• Subjects: disease resistance; Gene silencing; Homeobox; Infections; Jasmonic acid; Leucine; Leucine zipper proteins; lncRNA; miRNA; Modules; Mutants; Mutation; Non-coding RNA; Phenotypes; Phytophthora infestans; Point mutation; Ribonucleic acid; RNA; Solanum lycopersicum; target gene; tomato; Tomatoes; Phytophthora infestans; miRNA; lncRNA; tomato; disease resistance; target gene
• ISSN: 1672-9072; 1744-7909
• DOI: 10.1111/jipb.13339

ABSTRACT The yield and quality of tomatoes (Solanum lycopersicum) is seriously affected by Phytophthora infestans. The long non‐coding RNA (lncRNA) Sl‐lncRNA39896 is induced after P. infestans infection and was previously predicted to act as an endogenous target mimic (eTM) for the microRNA Sl‐miR166b, which function in stress responses. Here, we further examined the role of Sl‐lncRNA39896 and Sl‐miR166b in tomato resistance to P. infestans. Sl‐miR166b levels were higher in Sl‐lncRNA39896‐knockout mutants than in wild‐type plants, and the mutants displayed enhanced resistance to P. infestans. A six‐point mutation in the region of Sl‐lncRNA39896 that binds to Sl‐miR166b disabled the interaction, suggesting that Sl‐lncRNA39896 acts as an eTM for Sl‐miR166b. Overexpressing Sl‐miR166b yielded a similar phenotype to that produced by Sl‐lncRNA39896‐knockout, whereas silencing of Sl‐miR166b impaired resistance. We verified that Sl‐miR166b cleaved transcripts of its target class III homeodomain‐leucine zipper genes SlHDZ34 and SlHDZ45. Silencing of SlHDZ34/45 decreased pathogen accumulation in plants infected with P. infestans. Additionally, jasmonic acid and ethylene contents were elevated following infection in the plants with enhanced resistance. Sl‐lncRNA39896 is the first known lncRNA to negatively regulate resistance to P. infestans in tomato. We propose a novel mechanism in which the lncRNA39896–miR166b–HDZ module modulates resistance to P. infestans. The lncRNA Sl‐lncRNA39896 negatively regulates tomato resistance to Phytophthora infestans by sequestering the microRNA Sl‐miR166b, thus affecting the expression of Sl‐miR166b target HD‐Zip III transcription factors.