Integrated Sphingolipidomic and Transcriptomic Analysis Reveals Resistance Mechanisms to Bacterial Wilt in Peanut Varieties with Contrasting Tolerance

Abstract

Bacterial wilt, caused by the bacterium Ralstonia solanacearum, is a devastating disease that limits peanut production. The molecular mechanisms that distinguish between resistant and susceptible responses are being continuously explored; however, there is limited data with regard to the interaction between lipid metabolism and transcriptional reprogramming. Here we performed integrated sphingolipidomics and transcriptomics on the roots of the resistant peanut variety Zhonghua 6 (ZH6) and the susceptible variety Zhonghua 12 (ZH12) at pre-disease, early-onset, and late stages of infection. The resistant ZH6 variety exhibited the early accumulation of specific glucosylceramides (GluCer t18:1/h25:0 and GluCer t18:0/h23:0) and inositol phosphoceramide (IPC t18:0/h24:0). Metabolic stabilization occurred, with no significant lipid changes observed between the early and late stages. This response was supported by transcriptional activation of fatty acid α-hydroxylase (0538LJ), neutral/alkaline ceramidases (IX12GR, KZ47MP.1), and ABA signaling components (ABA receptor, SRK2A-like). In contrast, susceptible ZH12 displayed progressive sphingosine depletion and delayed accumulation of VLCFA-ceramide d18:0/16:0 and sterols. KCS4 was upregulated in ZH12, providing a transcriptional basis for VLCFA-ceramide accumulation. Hormone signaling divergence was evident: ZH6 exhibited early ABA signaling, followed by transcriptional stasis, whereas ZH12 displayed delayed ACS4/ACS11 hyper-induction after pathological ceramide accumulation. This was accompanied by auxin depletion (GH3.9 upregulation), failure of the cytokinin phosphorelay (HPt6 suppression), and decoupling of SA signaling (PR-1 induction without TGA activation). Resistance is therefore defined by early, coordinated sphingolipid remodeling and ABA signaling leading to homeostatic stabilization. In contrast, susceptibility represents delayed ceramide accumulation and multi-hormone signaling suppression. This multi-omics framework provides detailed lipidomic and transcriptomic signatures to identify candidate genes and lipid biomarkers for marker-assisted breeding of bacterial wilt-resistant peanut varieties.