Elevating herbivore‐induced JA‐Ile enhances potato resistance to the polyphagous beet armyworm but not to the oligophagous potato tuber moth

Abstract Background The oligophagous potato tuber moth (PTM), Phthorimaea operculella , and the polyphagous beet armyworm (BAW), Spodoptera exigua , are two destructive pests of potato, and infestations can lead to serious reduction in potato yield. However, potato plant responses to the two herbivories are only poorly understood. Endogenous jasmonoyl‐isoleucine (JA‐Ile) is a signal responsible for the induction of plant anti‐herbivore defenses. Elevation of JA‐Ile by blocking its catabolism is considered to be an effective and sustainable approach to enhance plant resistance to insect pests. However, it is not clear whether this approach can enhance potato resistance to PTM and BAW. Results We demonstrated that the transcriptional changes induced by simulated PTM and BAW feeding overlap to a large extent, and that 81.5% of the PTM‐ and 90.5% of the BAW‐responsive genes were commonly regulated. We also generated potato transgenic lines, irStCYP94B3s, in which the three JA‐Ile hydroxylases were all simultaneously silenced. These lines exhibited enhanced resistance only to BAW, but not to PTM, although levels of JA‐Ile and its downstream induced defensive chemicals, including caffeoylputrescine, dicaffeoylspermidine, lyciumoside II, and the nicotianosides I, II, and VII, were all present at higher levels in PTM‐infested than in BAW‐infested irStCYP94B3s lines. Conclusion Our results provide support for the hypothesis that StCYP94B3 genes are able to act as potential targets for the control of polyphagous insect pests in potato, and reveal that the oligophagous PTM has evolved an effective mechanism to cope with JA‐Ile‐induced anti‐herbivore defenses. © 2022 Society of Chemical Industry.