Overexpression of GhAAP3 increases Helicoverpa armigera feeding by altering hormonal and metabolic composition in cotton

GhAAP3 negatively regulates cotton resistance to Helicoverpa armigera by downregulating key defense pathways, impairing the plant's chemical defense, and enhancing nutritional suitability for herbivorous pests. Cotton (Gossypium spp.), a fundamental global fiber crop, is highly susceptible to insect pests, including Helicoverpa armigera. Amino acid/auxin permeases (AAAPs) are crucial membrane transporters involved in plant development and stress responses. In this study, we overexpressed amino acid permease 3 (GhAAP3) in upland cotton to evaluate its function in defense against H. armigera. The larvae fed on GhAAP3-overexpressing plants (AP3-1 and AP3-2) exhibited higher growth and feeding by 95.85% and 220.83%, respectively, compared to larvae fed on wild-type (WT) plants. Transcriptomic analysis revealed global downregulation of key defense pathways, including jasmonic acid (JA) biosynthesis and signaling, mitogen-activated protein kinase (MAPK) signaling, and phenylpropanoid and terpenoid biosynthesis pathways, in AP3. Consistently, GhAAP3 overexpression caused a marked reduction in JA-related hormones (JA, methyl jasmonate (MeJA), and jasmonic acid-isoleucine (JA-Ile)) by 45.75-87.41% and key defensive secondary metabolites (flavonoids and gossypol) by 26.35-56.38%. Conversely, free amino acids and soluble sugar contents increased significantly in AP3-overexpressing transgenic plants. Our findings demonstrate that GhAAP3 negatively regulates cotton resistance against H. armigera by downregulating key defense-related phytohormones and secondary metabolites, while concurrently elevating amino acid and sugar levels. This together impairs the plant's chemical defense and enhances its nutritional suitability for herbivorous pests.