Integrated physiological, transcriptome and metabolome analysis revealed the response mechanisms of melon to Podosphaera xanthii
Yanyan Cao, Dongwei Yao, Qiannan Diao, Shoubo Tian, Dan Lv, Wenxian Zhang, Yongping Zhang
Abstract
• Integrated multi-omics approaches were applied for studying the PM response of melon. • The resistant melon exhibited superior antioxidant enzyme activities. • A JA-lipid synergy was pivotal for powdery mildew resistance. • Defense involved a complex multi-hormone signaling network. • Key TFs including ERF and WRKY orchestrated the immune response. Powdery mildew (PM), caused by Podosphaera xanthii ( P. xanthii ), is a devastating disease in melon worldwide. However, the molecular mechanisms that govern the host response and confer effective resistance remain poorly understood. Through an integrated multi-omics analysis of resistant (J152) and susceptible (J156) melon lines, we found that a broad spectrum of defense pathways, including MAPK signaling, plant-pathogen interactions, linoleic and alpha-linolenic acid metabolism, plant hormone signal transduction, and transcription factors (e.g., ERF, MYB, WRKY, bHLH, NAC, and bZIP), were transcriptionally activated in both genotypes upon infection. Although physiological responses such as increased antioxidant enzyme activities and the accumulation of oxidative stress markers (MDA and H₂O₂) occurred in both lines, these responses were significantly stronger and more efficient in J152. The critical distinction was the specific and efficient coordination of a subordinate network in the resistant line, centered on a highly synergistic interplay between the reprogramming of lipid metabolism and a jasmonic acid (JA)-centric hormone signaling network, wherein JA likely functions as a core hub mediating crosstalk with other hormones. This core module amplified the antioxidant capacity and effectively mitigated oxidative damage, resulting in superior maintenance of membrane integrity in J152. Conversely, J156 exhibited a dysregulated induction of the same pathways, which failed to coordinate an effective defense, leading to higher oxidative damage. Our study establishes that the specific synergy between lipid metabolism and a JA-centric hormone network is a pivotal mechanism conferring PM resistance in melon, providing potential targets for breeding programs and disease management strategies.