Proteomic and transcriptional regulations in Theobroma cacao L., in response to Ni toxicity, reveal temporal and metabolic reprogramming.

Nickel (Ni) toxicity adversely impacts plant metabolism, reducing the productivity and quality of cacao (Theobroma cacao) beans, posing significant challenges to its grown. Additionally, Ni accumulation in cacao beans raises concerns regarding food safety and human health. To elucidate the metabolic and molecular responses of cacao trees to soil Ni contamination, an integrative analysis combining proteomics, transcriptional, and protein-protein interaction network studies was conducted. The study evaluated responses over two-time intervals and across a gradient of soil Ni concentrations. Across all treatments, a total of 688 proteins were identified. After statistical filtering, 238 DAPs were identified at 24 h and 308 DAPs at 96 h. Early responses included upregulation of 87 proteins, primarily involved in energy metabolism and antioxidant defense, and downregulation of 135 proteins associated with photosynthesis and chloroplast organization. At 96 h, 126 proteins were upregulated, while 267 were downregulated, with shifts toward photosynthesis restoration and biosynthetic processes. Gene expression analysis revealed increased expression of genes SOD-Chl (35 %), SOD-Cyt (42 %) and PER-1 (39 %), related to oxidative stress, PCS (55 %) related to detoxification, and psbA (52 %) and psbD (49 %) related to photosynthesis at 24 h, with persistence at 96 h. The PPI networks revealed distinct functional clusters, including ROS detoxification and photosynthetic repair hubs. This research offers an in-depth analysis of the dynamic and multifaceted strategies employed by T. cacao to mitigate Ni-induced toxicity. These findings offer valuable insights for developing future breeding programs aimed at enhancing cacao resilience to heavy metal stress.