Cadmium-mediated totradexicity in plant cells is associated with the DCD/NRP-mediated cell death response

Cadmium (Cd2+) is highly harmful to plant growth. Although Cd2+ induces programmed cell death (PCD) in plant cells, Cd2+ stress in whole plants during later developmental stages and the mechanism underlying Cd2+-mediated toxicity are poorly understood. Here, we showed that Cd2+ limits plant growth, causes intense redness in leaf vein, leaf yellowing, and chlorosis during the R1 reproductive stage of soybean (Glycine max). These symptoms were associated with Cd2+-induced PCD, as Cd2+-stressed soybean leaves displayed decreased number of nuclei, enhanced cell death, DNA damage, and caspase 1 activity compared to unstressed leaves. Accordingly, Cd2+-induced NRPs, GmNAC81, GmNAC30 and VPE, the DCD/NRP-mediated cell death signalling components, which execute PCD via caspase 1-like VPE activity. Furthermore, overexpression of the positive regulator of this cell death signalling GmNAC81 enhanced sensitivity to Cd2+ stress and intensified the hallmarks of Cd2+-mediated PCD. GmNAC81 overexpression enhanced Cd2+-induced H2O2 production, cell death, DNA damage, and caspase-1-like VPE expression. Conversely, BiP overexpression negatively regulated the NRPs/GmNACs/VPE signalling module, conferred tolerance to Cd2+ stress and reduced Cd2+-mediated cell death. Collectively, our data indicate that Cd2+ induces PCD in plants via activation of the NRP/GmNAC/VPE regulatory circuit that links developmentally and stress-induced cell death.