ERF Transcription Factor NaERF_IDOG Regulates JA-Induced Defence and Growth Inhibition in Nicotiana attenuata Upon...

Jasmonate (JA) regulates defence responses in plants. However, JA-induced defence often results in growth inhibition. This process is largely mediated by MYC2, the master regulator of JA signalling. Nevertheless, the underlying molecular mechanisms have not yet been fully uncovered. Here, we discovered that the ERF transcription factor NaERF_IDOG plays a key role in the JA-induced defence over growth in Nicotiana attenuata upon infection by the notorious fungal pathogen Alternaria alternata. NaERF_IDOG expression was directly controlled by JA through NaMYC2a/b. Plants silenced or knocked out for either NaERF_IDOG or both NaMYC2a and NaMYC2b exhibited similar phenotypes: they were both more vulnerable to A. alternata but grew larger. However, stable overexpression of NaERF_IDOG increased resistance to the fungus and reduced growth in both wild-type (WT) plants and those co-silenced with NaMYC2a/b to a similar extent. Further analysis indicated that NaERF_IDOG binds directly to the promoters of the biosynthetic genes for scopoletin, JA and GA, including NaF6'H1, NaAOS and NaKAO1-like, thereby activating scopoletin and JA biosynthesis while suppressing GA biosynthesis. Finally, our results revealed that both increasing scopoletin levels and reducing GA biosynthesis were involved in JA-induced disease resistance and growth inhibition. Thus, our study revealed how JA prioritizes defence against A. alternata over growth by a novel regulatory network, JA-MYC2-ERF_IDOG-Scopoletin/JA/GA. These findings provide new insights into the molecular mechanisms underlying the trade-off between defence and growth in plants and highlight the key role of NaERF_IDOG in the biosynthesis of scopoletin, JA and GA.