Cotton Bollworm (H. armigera) Effector PPI5 Targets FKBP17‐2 to Inhibit ER Immunity and JA/SA Responses, Enhancing Insect Feeding

Abstract The cotton bollworm causes severe mechanical damage to plants during feeding and leaves oral secretions (OSs) at the mechanical wounds. The role these OSs play in the invasion of plants is still largely unknown. Here, a novel H. armigera effector peptidyl prolyl trans‐isomerase 5 (PPI5) was isolated and characterized. PPI5 induces the programmed cell death (PCD) due to the unfolded protein response (UPR) in tobacco leaf. We reveal that PPI5 is important for the growth and development of cotton bollworm on plants, as it renders plants more susceptible to feeding. The GhFKBP17‐2, was identified as a host target for PPI5 with peptidyl‐prolyl isomerase (PPIase) activity. CRISPR/Cas9 knock‐out cotton mutant ( CR‐GhFKBP17‐1/3 ), VIGS ( TRV: GhFKBP17‐2 ) and overexpression lines ( OE‐GhFKBP17‐1/3 ) were created and the data indicate that GhFKBP17‐2 positively regulates endoplasmic reticulum (ER) stress‐mediated plant immunity in response to cotton bollworm infestation. We further confirm that PPI5 represses JA and SA levels by downregulating the expression of JA‐ and SA‐associated genes, including JAZ3/9 , MYC2/3 , JAR4 , PR4 , LSD1 , PAD4 , ICS1 and PR1/5 . Taken together, our results reveal that PPI5 reduces plant defense responses and makes plants more susceptible to cotton bollworm infection by targeting and suppressing GhFKBP17‐2 ‐mediated plant immunity.