JRE 4 is a master transcriptional regulator of defense‐related steroidal glycoalkaloids in tomato

• Published in: The Plant journal : for cell and molecular biology 2018-06, Vol.94 (6), p.975-990
• Main Authors: Nakayasu, Masaru, Shioya, Naoki, Shikata, Masahito, Thagun, Chonprakun, Abdelkareem, Ayman, Okabe, Yoshihiro, Ariizumi, Tohru, Arimura, Gen‐ichiro, Mizutani, Masaharu, Ezura, Hiroshi, Hashimoto, Takashi, Shoji, Tsubasa
• Format: Article
• Language: English
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.13911

Steroidal glycoalkaloids ( SGA s) are specialized anti‐nutritional metabolites that accumulate in Solanum lycopersicum (tomato) and Solanum tuberosum (potato). A series of SGA biosynthetic genes is known to be upregulated in Solanaceae species by jasmonate‐responsive Ethylene Response Factor transcription factors, including JRE 4 (otherwise known as GAME 9), but the exact regulatory significance in planta of each factor has remained unaddressed. Here, via TILLING ‐based screening of an EMS ‐mutagenized tomato population, we isolated a JRE 4 loss‐of‐function line that carries an amino acid residue missense change in a region of the protein important for DNA binding. In this jre4 mutant, we observed downregulated expression of SGA biosynthetic genes and decreased SGA accumulation. Moreover, JRE 4 overexpression stimulated SGA production. Further characterization of jre4 plants revealed their increased susceptibility to the generalist herbivore Spodoptera litura larvae. This susceptibility illustrates that herbivory resistance is dependent on JRE 4 ‐mediated defense responses, which include SGA accumulation. Ethylene treatment attenuated the jasmonate‐mediated JRE 4 expression induction and downstream SGA biosynthesis in tomato leaves and hairy roots. Overall, this study indicated that JRE 4 functions as a primary master regulator of SGA biosynthesis, and thereby contributes toward plant defense against chewing insects. Based on analysis of a mutant of JRE4 with impaired DNA‐binding activity, we show that this ERF transcription factor functions in tomato as a primary master regulator of SGA biosynthesis and contributes towards plant defense against chewing insects.