Bean plant receptor links caterpillar attack to predatory wasps

The common bean uses an immune receptor to recognize chemical signals left by caterpillars during feeding and trigger the release of volatiles capable of attracting predatory wasps. The mechanism involves the INR receptor, present in the leaves of the bean Phaseolus, and the peptide inceptin, found in the oral secretions of caterpillars. Laboratory and field trials in Mexico have shown a link between molecular recognition of herbivory, plant defense, and the recruitment of natural enemies.

The study evaluated tritrophic interactions between plants, herbivorous insects, and predators. Scientists demonstrated that INR recognizes inceptin and activates specific responses in the common bean. These responses amplify the reaction to injury and induce an immune pathway associated with herbivory. The result includes the release of a characteristic mixture of volatile compounds. This mixture guided predatory wasps to the attacked plants.

Comparison of lineages

The team compared bean lines with a functional receptor and lines with a natural mutation in the INR gene. The mutation was named inr-1. It involves a deletion of 103 base pairs in the PvINR locus. This alteration generates a truncated protein and impairs the perception of inceptin.

In initial tests, the PI 311785 cell line responded to inceptin application with ethylene accumulation and volatile emission. The W6 13807 cell line did not show the same response. The analysis also indicated activation of MAPK3 and MAPK6 in PI 311785 after fifteen minutes of inceptin treatment. This phosphorylation did not occur in W6 13807. The result indicated a failure in the inceptin-specific signaling cascade.

Near-isogenic strains allowed the isolation of the mutation effect. inr-1/inr-1 plants did not produce inceptin-induced ethylene. Even so, they maintained a response to the bacterial peptide flg22. This data indicates that insensitivity to inceptin did not result from a general failure in the plant's immune system.

Direct defense

The mutation also reduced direct defense against herbivory. Larvae of Spodoptera exigua grew 72,7 percent more in INR-1/INR-1 plants than in INR/INR sister plants during five days of feeding. This result indicates the participation of the functional receptor in the resistance of the common bean to caterpillars.

The molecular response included transcriptional reprogramming. In Phaseolus cv. Red hawk, the treatment with wounding and inceptin induced 527 genes compared to wounding with water. Some of these genes were related to protein phosphorylation and transcription regulation. Transcription factors from the ERF, WRKY, bHLH, MYB, and bZIP families, linked to defenses against herbivores, also appeared.

Emission of volatiles

The emission of volatiles depended on the receptor. INR/INR cell lines treated with inceptin or oral secretions of Spodoptera frugiperda emitted a typical mixture of volatile compounds induced by herbivory. Among the compounds, the study highlighted DMNT, methyl salicylate, and TMTT. Inr-1/inr-1 plants did not emit this typical mixture. They released compounds associated with isolated injury.

The field tests took place in a 925-square-meter agricultural area near Bajos de Chila, in Oaxaca, Mexico, during the experimental growing seasons of 2023 and 2024. The scientists used sentinel caterpillars of Spodoptera frugiperda attached to bean leaves. The plants were wounded with water, oral secretions from caterpillars, or inceptin at physiological concentration.

Wasp visits occurred in both years. Visitation rates to the treatments ranged from 55,1 percent to 86,9 percent. In 2023, plants with the inr-1/inr-1 mutation treated with oral secretions showed a 40 percent reduction in wasp attacks of the genera i>Polybia and Mischocyttarus to sentinel caterpillars. In 2024, the application of inceptin also resulted in a 40 percent reduction in attacks on inr-1/inr-1 plants. In the water treatment, there was no difference in visitation.

The results indicate that the INR receptor connects caterpillar detection to predator recruitment in common beans. The study also points to agronomic relevance for systems with legumes, such as milpa and push-pull intercropping. According to the scientists, the evolutionary distribution of INR in phaseoloid legumes may help explain the indirect defense mediated by volatiles in these systems.

Further information can be found at doi.org/10.1126/sciadv.aec3229