Enhanced photosynthetic carbon assimilation and optimized carbon partitioning drive Cd-induced hormetic growth in the hyperaccumulator Celosia argentea

The molecular mechanisms underlying cadmium (Cd)-induced hormesis in plants are poorly understood, in stark contrast to the well-characterized pathways of Cd toxicity. Hyperaccumulators, with their inherently higher Cd tolerance threshold, provide ideal models for investigating this phenomenon. Here, we used the Cd hyperaccumulator Celosia argentea to uncover the molecular basis of hormetic growth induced by low-level Cd (0.3 μmol L⁻¹). This treatment increased aboveground biomass by 30%, chlorophyll a content by 34.6%, Rubisco activity by 111.2%, and significantly enhanced photosynthetic efficiency (Pn, qP, and ETR). Transcriptome analysis revealed that low-level Cd upregulated a coordinated set of genes involved in chlorophyll biosynthesis (e.g., ChlHM, CLA1 ), photosystem II assembly ( psbQ, psbP, psbR ), photosynthetic electron transport ( petE, petH ), and photosystem I components ( psaB, psaN ). These changes enhanced chlorophyll biosynthesis and light reaction efficiency, thereby improving photosystem stability and biomass production. Concurrently, Cd induced carbohydrate reallocation: the contents of total sugar, soluble sugar, and sucrose were increased by 20.4%, 38.4%, and 49.1%, respectively, while starch content was decreased by 48.3%. Starch synthase activity was decreased by 13.1%, whereas sucrose synthase activity was increased by 43.2%. Accordingly, the sucrose synthesis gene SPS was upregulated, whereas the starch synthesis gene AGPase was downregulated. Thus, low-level Cd transcriptionally reprograms photosynthate partitioning from starch toward soluble sugars, channeling more carbon toward growth. Collectively, our findings reveal that low-level Cd orchestrates a multi-pathway transcriptional response—enhancing photosynthesis and redirecting carbon flux—to promote growth in C. argentea , providing novel molecular insights into Cd-induced hormesis in plants.