An effector from cotton bollworm oral secretion impairs host plant defense signaling

Significance Plants recognize insect-derived molecules and make the accurate defense response during herbivory. However, insects release effectors that disturb host plant defense responses for fitness. Effectors are crucial components in biotic interactions. We identified a caterpillar-derived effector (HARP1) from oral secretion of cotton bollworm, a devastating agricultural pest. HARP1 is released from larvae to plant leaves during feeding and is able to migrate from wounding site into plant cells automatically. HARP1 interacts with JASMONATE-ZIM-domain (JAZ) proteins, the suppressor of Jasmonate (JA) pathway, and blocks signaling transduction by preventing JAZ degradation. HARP1-like proteins are widely distributed and have conserved function in noctuids, and they may contribute to insect adaptation to host plants during coevolution.
Insects have evolved effectors to conquer plant defense. Most known insect effectors are isolated from sucking insects, and examples from chewing insects are limited. Moreover, the targets of insect effectors in host plants remain unknown. Here, we address a chewing insect effector and its working mechanism. Cotton bollworm (Helicoverpa armigera) is a lepidopteran insect widely existing in nature and severely affecting crop productivity. We isolated an effector named HARP1 from H. armigera oral secretion (OS). HARP1 was released from larvae to plant leaves during feeding and entered into the plant cells through wounding sites. Expression of HARP1 in Arabidopsis mitigated the global expression of wounding and jasmonate (JA) responsive genes and rendered the plants more susceptible to insect feeding. HARP1 directly interacted with JASMONATE-ZIM-domain (JAZ) repressors to prevent the COI1-mediated JAZ degradation, thus blocking JA signaling transduction. HARP1-like proteins have conserved function as effectors in noctuidae, and these types of effectors might contribute to insect adaptation to host plants during coevolution.