Stemborer‐induced rice plant volatiles boost direct and indirect resistance in neighboring plants

Abstract

Summary Herbivore‐induced plant volatiles (HIPVs) are known to be perceived by neighboring plants, resulting in induction or priming of chemical defenses. There is little information on the defense responses that are triggered by these plant–plant interactions, and the phenomenon has rarely been studied in rice. Using chemical and molecular analyses in combination with insect behavioral and performance experiments, we studied how volatiles emitted by rice plants infested by the striped stemborer (SSB) Chilo suppressalis affect defenses against this pest in conspecific plants. Compared with rice plants exposed to the volatiles from uninfested plants, plants exposed to SSB‐induced volatiles showed enhanced direct and indirect resistance to SSB. When subjected to caterpillar damage, the HIPV‐exposed plants showed increased expression of jasmonic acid (JA) signaling genes, resulting in JA accumulation and higher levels of defensive proteinase inhibitors. Moreover, plants exposed to SSB‐induced volatiles emitted larger amounts of inducible volatiles and were more attractive to the parasitoid Cotesia chilonis. By unraveling the factors involved in HIPV‐mediated defense priming in rice, we reveal a key defensive role for proteinase inhibitors. These findings pave the way for novel rice management strategies to enhance the plant's resistance to one of its most devastating pests.

Comparative analysis of sorghum (C4) and rice (C3) plant headspace volatiles induced by artificial herbivory

“…In spite of qualitative overlap between volatile blends of rice and sorghum (Table S1, Figures 3, 5 , S2), 13 , 34 , 35 significantly higher levels of induced VOCs were typical for rice. In addition, low levels of basal volatiles emitted from sorghum support the idea of sorghum being a low emitter rather than being a low responder to herbivory stimuli.…”

Functional analysis of odorant-binding proteins for the parasitic host location to implicate convergent evolution between the grain aphid and its parasitoid Aphidius gifuensis

“…The olfactory perception in insects as well as other animals is generally dose-dependent. Dose beyond the threshold range, either too high or too low, will lead to a decrease in response [81]. Thus, the up-regulation induced by low-dose EBF, i.e., 40 ng, suggested that AgifOBP9 was associated with the high sensitivity of aphidius to EBF.…”

Defense Strategies of Rice in Response to the Attack of the Herbivorous Insect, Chilo suppressalis

“…By analyzing the levels of JA and SA in ir- lrr rice and WT plants after SSB attack and mechanical damage, it can be concluded that OsLRR-RLK1 does not regulate the production of trauma-induced JA, JA-Ile, and SA in the absence of SSB attack [ 52 ]. Healthy rice plants were exposed to SSB-induced rice volatiles, and two JA signaling genes ( DOX2 and LOX8 ) were directly induced, resulting in a significant increase in JA accumulation [ 79 ]. The absence of OM64 in rice stimulates SSB-induced JA biosynthesis and response, enhancing the resistance of rice to the SSB [ 61 ].…”

“…When rice is attacked by the SSB, it can release a significant amount of (Z)-3-hexene-1-ol, which serves as an attractant for natural enemy parasitic wasps that parasitize SSB larvae. Similarly, other substances emitted by rice, such as linalool (terpenoids) or ethyl benzoate, methyl salicylate-4, 8-dimethyl-1, 3, 7-nonanetriene (DMNT), can also attract the arrival of parasitic wasps, thereby participating in the defense of rice against the SSB [ 79 , 80 ].…”

“…More importantly, after overexpression of the AvrPiz-t interacting protein 4 ( APIP4 ) gene in rice, the accumulation of trypsin protease inhibitor increased, and the weight of the SSB fed with APIP4 strains significantly decreased (compared with WT), while the performance of knockout strains ( apip4-5 ) was the opposite [ 76 ]. In addition, the accumulation and activity level of trypsin plays a central role in all studies that have shown enhanced resistance of rice to the SSB [ 52 , 62 , 65 , 66 , 67 , 77 , 79 , 80 ].…”