Constitutive and inducible tomato defenses contribute to Bacillus thuringiensis lethality against Spodoptera exigua

Abstract

In nature, insect herbivory exerts continuous selective pressure on plants that, in turn, have developed a wide array of constitutive and inducible defenses to fight against attackers. Since plant defenses may affect higher trophic levels, including entomopathogens, further research is required to understand how plant compounds influence insect-pathogens interactions and their implications for integrated pest management programs. Here, we evaluated the impact of tomato defenses on the lethality produced by the bacterial entomopathogen Bacillus thuringiensis (Bt) against second instar larvae of Spodoptera exigua. We first examined the effect of constitutive defenses from fifteen wild tomato species and forty cultivated varieties (Solanum lycopersicum) on S. exigua larval growth and susceptibility to Bt. The results showed larvae fed on wild tomato species had a reduced larval growth compared to larvae fed on cultivated varieties, whereas susceptibility to Bt was similar between both groups. We then selected six cultivated varieties, including those with high and low impacts on larval growth and Bt-induced mortality, to further explore the effect of inducible defenses. Elicitation of defenses by methyl jasmonate (MeJA) reduced larval growth and increased basal mortality. Additionally, when larvae were infected with Bt, MeJA treatment further increased their susceptibility to the entomopathogen. Metabolomic analysis confirmed a reprogramming of tomato leaf metabolism following MeJA elicitation, with an induced accumulation of bioactive compounds, such as saponins or flavonoids, known for their anti-herbivory properties in most tomato varieties. Overall, these data reveal that both constitutive and inducible tomato defenses not only protect the plant by directly affecting the insect pest but also enhance the efficacy of bacterial entomopathogens.