Multifunctionality of Jasmonic Acid Accumulation during Aphid Infestation in Altering the Plant Physiological Traits That Suppress the Plant Defenses in Wheat Cultivar XN979

SIMPLE SUMMARY: Our previous study demonstrated that previous aphid infestation significantly upregulates the transcription of marker genes associated with salicylic acid (SA) and jasmonic acid (JA) biosynthesis. However, accumulating experimental evidence has revealed that SA and JA signaling cascades in plant immune responses always act antagonistically across a diverse range of herbivore–plant systems. In this study, we determined the potential role of JA in suppressing plant defense responses in seedlings of the wheat cultivar XN979 through preference and performance experiments using grain aphids and evaluated the underlying mechanisms through the transcriptional profiles of marker genes related to JA- and SA-dependent responses and the formation of tryptamine. The obtained results reveal that the accumulation of JA during aphid infestation probably facilitates the forming of tryptamine, which is then probably converted into IAA or serotonin to alter the plant’s physiological properties and facilitate the feeding behaviors of aphids, compensating for the adverse effects of SA- or JA-dependent responses in host plants to colonizer attacks. As a result of this experiment, we have a better understanding of the antagonistic interactions between hormone signaling processes. ABSTRACT: Crop plants have coevolved phytohormone-mediated defenses to combat and/or repel their colonizers. The present study determined the effects of jasmonic acid (JA) accumulation during aphid infestation on the preference and performance of Sitobion miscanthi Takahashi (Hemiptera: Aphididae), and its potential role in fine-tuning hormone-dependent responses in XN979 wheat cultivar seedlings was evaluated via the transcriptional profiles of marker genes related to JA- and salicylic acid (SA)-dependent responses. The preference experiment and the life table data reveal that direct foliage spraying of 2.5 mM methyl jasmonate (MeJA) exhibited weak negative or positive effects on the preferential selection and the population dynamics and oviposition parameters of S. miscanthi. The transcription level of phytohormone biosynthesis genes shows that foliage spraying of MeJA significantly upregulated the marker genes in the JA biosynthesis pathway while downregulating the SA pathway. In addition, either MeJA treatment or previous aphid infestation significantly induced upregulated transcription of the genes involved in the JA- and SA-dependent defense responses, and the transcription level of the tryptophan decarboxylase (TaTDC) gene, which facilitates the conversion of L-tryptophan to tryptamine, was rapidly upregulated after the treatments as well. The main products of tryptamine conversion could play a crucial role in suppressing SA-dependent defense responses. These results will provide more experimental evidence to enable understanding of the antagonistic interaction between hormone signaling processes in cereals under aphid infestation.