Cobalt and nickel reduce maize growth through different tissue-specific pathways

Heavy metals contamination of soils is an increasing environmental problem and impairs crop yields and food safety. However, the scientific understanding of the mechanisms by which cobalt (Co) and nickel (Ni) induce growth inhibition remains limited, particularly with regard to organ-specific responses and the impact of combined metal exposure. To resolve these discrepancies, analyses were conducted of maize responses to Co-, Ni-, and Co/Ni-stress using integrated physiological, biochemical, and transcriptomic approaches. Both metals reduced plant growth, but through different processes. Ni predominantly impaired root elongation, while Co caused a greater decrease in chlorophyll content and negatively affected leaf functionality. Metal treatments disrupted micronutrient homeostasis, particularly that of manganese in plants treated with Co. Treatment with Co and Ni also triggered oxidative stress in both leaves and roots. The physiological and biochemical changes in maize treated with Co and Ni were accompanied with changes in gene expression. The number of differentially expressed genes was significantly higher in the roots than in the shoots, which is probably due to the higher content of Co and Ni in the root. Differentially expressed genes were enriched in categories related to manganese homeostasis, metal transport, oxidative stress responses, and cell wall organization. Overall, Co and Ni decreased maize growth, but by affecting different physiological and molecular processes. The combined Co/Ni treatment revealed both additive (e.g. root biomass) and non-additive effects (e.g. shoot biomass). Our study undercovers these different molecular processes and highlights the importance of considering metal- and tissue-specific responses. • Co and Ni elicit distinct organ-specific physiological and transcriptomic responses • Co impairs leaf metabolism mainly by reducing manganese and chlorophyll content • Ni inhibits root elongation more strongly and impairs cell wall synthesis • Both metals disrupt metal homeostasis and cause oxidative stress • The combined effect of Co and Ni is not simply the sum of their individual effects