Integrated Omics Analysis Reveals Key Pathways in Cotton Defense against Mirid Bug (Adelphocoris suturalis Jakovlev) Feeding

Simple Summary: This study delves into the intricate defense mechanisms of cotton plants against the primary pest Adelphocoris suturalis Jakovlev, which has become a major concern in Bt-cotton fields. Through advanced analytical techniques, this study identified specific changes in the cotton plant's metabolism and protein expression triggered by A. suturalis feeding. These findings revealed a notable increase in the expression of certain alpha-linolenic acid metabolism pathway-related proteases and a simultaneous decrease in fructose and mannose biosynthesis-related proteases. These molecular responses shed light on the complex interplay between cotton plants and A. suturalis. Therefore, this study not only deepens our understanding of plant-insect interactions but also provides valuable insights for developing innovative strategies to control this cotton pest, thereby offering potential solutions for sustainable cotton cultivation. The recent dominance of Adelphocoris suturalis Jakovlev as the primary cotton field pest in Bt-cotton-cultivated areas has generated significant interest in cotton pest control research. This study addresses the limited understanding of cotton defense mechanisms triggered by A. suturalis feeding. Utilizing LC-QTOF-MS, we analyzed cotton metabolomic changes induced by A. suturalis, and identified 496 differential positive ions (374 upregulated, 122 downregulated) across 11 categories, such as terpenoids, alkaloids, phenylpropanoids, flavonoids, isoflavones, etc. Subsequent iTRAQ-LC-MS/MS analysis of the cotton proteome revealed 1569 differential proteins enriched in 35 metabolic pathways. Integrated metabolome and proteome analysis highlighted significant upregulation of 17 (89%) proteases in the alpha-linolenic acid (ALA) metabolism pathway, concomitant with a significant increase in 14 (88%) associated metabolites. Conversely, 19 (73%) proteases in the fructose and mannose biosynthesis pathway were downregulated, with 7 (27%) upregulated proteases corresponding to the downregulation of 8 pathway-associated metabolites. Expression analysis of key regulators in the ALA pathway, including allene oxidase synthase (AOS), phospholipase A (PLA), allene oxidative cyclase (AOC), and 12-oxophytodienoate reductase3 (OPR3), demonstrated significant responses to A. suturalis feeding. Finally, this study pioneers the exploration of molecular mechanisms in the plant-insect relationship, thereby offering insights into potential novel control strategies against this cotton pest.