bHLH090 promotes insect resistance by positively regulating myrosin idioblast development and myrosinase biosynthesis

The glucosinolate-myrosinase system is vital for chemical defense against herbivory and pathogen infection in Brassicales plants. Myrosinase, which catalyzes the hydrolysis of glucosinolates into toxic compounds, accumulates to high levels in the vacuoles of myrosin idioblast cells (MIs) when plants are attacked. Here, we showed that the transcription factor bHLH090 positively regulates the development of MIs and the biosynthesis of myrosinase in Arabidopsis (Arabidopsis thaliana). bHLH090 was specifically expressed in the MIs of leaves, stems, and sepals. Weak bHLH090 expression in the bhlh090 T-DNA mutant resulted in fewer MIs developing in true leaves. Both expression of the myrosinase biosynthesis gene THIOGLUCOSIDE GLUCOHYDROLASE1 (TGG1) and myrosinase activity were lower in the bhlh090 mutant. By contrast, TGG1 expression and myrosinase activity were higher in bHLH090-overexpressing transgenic plants. In accordance with these results, bhlh090 mutant plants exhibited increased susceptibility to the herbivore Spodoptera exigua, while bHLH090 overexpression conferred greater resistance to S. exigua. Moreover, we determined that expression of bHLH090 in the MIs depends on the function of FAMA, a core regulator of MI development, as bHLH090 expression was not detected in the fama-1 loss-of-function mutant. We showed that FAMA binds directly to the promoter of bHLH090 and promotes bHLH090 expression. Additionally, bHLH090 physically interacts with FAMA, thereby augmenting its capacity to activate TGG1. Our results reveal a FAMA-bHLH090-TGG1 regulatory module involved in the regulation of MI development and myrosinase biosynthesis, as well as resistance to insect herbivores.