Depicting the Physiological, Biochemical and Metabolic Responses to the Removal of Adventitious Roots and Their Functions in Cucumis melo Under Waterlogging Stress

Waterlogging poses a grave abiotic stress that hampers crop productivity and survival due to reduced oxygen availability in the impacted tissues. To adapt to this hypoxic environment, the hypocotyls of melon (Cucumis melo L.) seedlings can produce a profusion of adventitious roots when exposed to waterlogging stress. However, research on the significance of these adventitious roots under waterlogging stress has been limited. The present study aimed to elucidate the critical role of adventitious roots by investigating the physiological, biochemical, and metabolic changes that occur following their removal during waterlogging stress. The removal of adventitious roots compromised the normal growth of melon seedlings, resulting in phenotypic abnormalities such as chlorotic and withered leaves. Our results indicated that the removal of adventitious roots led to significant reductions in total chlorophyll levels by 62.89% and 43.60% compared to the normal control condition and waterlogging stress alone, respectively. Additionally, in the adventitious root removal treatment, higher malondialdehyde (MDA) content, O2•− production rate, monodehydroascorbate reductase (MDHAR) activity, alcohol dehydrogenase (ADH) activity, the AsA/DHA ratio, proline content, jasmonic acid (JA) content, and 1-aminocyclopropane-1-carboxylic acid (ACC) content were observed. Specifically, JA levels were significantly enhanced by 180.54% and 52.05%, and ACC levels were significantly increased by 519.23% and 125.16% compared to the control and waterlogging stress conditions, respectively. Through untargeted metabolomic analysis, a total of 447 differentially accumulated metabolites (DAMs) were identified. Notably, jasmonic acid and brassinolide, which are involved in plant hormone signal transduction, along with cyanidin 3-(2G-xylosylrutinoside) classified as flavonoids, (2S,3′S)-α-amino-2-carboxy-5-oxo-1-pyrrolidinebutanoic acid categorized as proline and derivatives, and ligstroside-aglycone and foeniculoside VII annotated as terpenoids, exhibited key roles in the waterlogging response. This research enhances our understanding of the mechanisms underlying the removal of adventitious roots during waterlogging stress, as well as the associated physiological, biochemical, and metabolic changes. These findings provide valuable insights into the crucial role of adventitious roots in melon seedlings subjected to waterlogging stress and may inform strategies for enhancing waterlogging tolerance in breeding practices.