Comparative metabolomic and transcriptomic analysis revealing the role of salicylic acid for short-term response with arginine and myristic acid for long-term tolerance under salt stress in watermelon (Citrullus lanatus L.)

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Introduction: L.) is an important horticultural crop worldwide. Meanwhile, watermelon has a moderately tolerant susceptibility to salinity, making it an excellent model crop for studying salt stress-induced response and tolerance mechanism. Methods: Two watermelon homozygous inbred lines named 'HY17' (Salt-sensitive) and 'HY73' (Salt-tolerant) were used as materials. Seedlings at three-leaf age were treated with 150 mM NaCl for 2 days and 25 days to imitate short-term and long-term salt stress, respectively. Results: Comparative metabolomic and transcriptomic analysis combined with phenotypic stress indexes analysis revealed that higher biosynthesis of salicylic acid derived from the phenylalanine metabolism pathway in 'HY73' than 'HY17' is important for short-term response to salinity. Arginine and myristic acid accumulation, which is responsible for osmotic adjustment, reactive oxygen species (ROS) scavenging, and alleviating membrane lipid peroxidation, play roles in the tolerance to long-term salt stress in watermelon. Discussion: Differentially expressed genes (DEGs) of aspartate aminotransferase (AST: Cla97C04G073110 and Cla97C11G220050) and alanine transaminase (ALT: Cla97C09G163470 and Cla97C07G141140) are crucial for arginine biosynthesis, and the fatty acyl-ACP thioesterase B gene (FATB: Cla97C06G119690) is the key for myristic acid biosynthesis for improving salt tolerance. In addition, K+/Na+ transportation-related DEGs, including the high-affinity K+ transporter gene (HKT: Cla97C06G123400) and low-affinity K+ transporter gene (KT: Cla97C10G197240), and key members in salt overly sensitive (SOS) pathway (SOS2/CIPK: Cla97C02G045030 and SOS3/CBL: Cla97C06G127530) were identified as responsible for regulating intracellular ionic homeostasis as salinity resistance. Hence, these results highlight the holistic resistant mechanisms of short-term response and long-term tolerance under salt stress in watermelon.