Cadmium‐mediated toxicity in plant cells is associated with the DCD/NRP‐mediated cell death response

Abstract

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.

Excess Zinc Supply Reduces Cadmium Uptake and Mitigates Cadmium Toxicity Effects on Chloroplast Structure, Oxidative Stress, and Photosystem II Photochemical Efficiency in Salvia sclarea Plants

“…Salvia sclarea is recognized as a medicinal herb due to its valuable pharmacological properties and numerous health benefits, being also an economically important plant for phytoextraction and phytostabilization of Cd 2+ -and Zn 2+ -contaminated soils, with a subsequent increased interest in its cultivation [2,14,27]. Cadmium is greatly injurious to plant growth and almost all human individuals are exposed to Cd 2+ , mostly through plantderived food that has reached the threshold for adverse health effects, and therefore, there is a serious demand to lower human Cd 2+ intake by development of low Cd 2+ -accumulating crops [42,43]. In addition to food consumption, medicinal plants, and processed foods, Cd 2+ is naturally stored at high concentrations in cigarettes [42][43][44].…”

“…Cadmium is greatly injurious to plant growth and almost all human individuals are exposed to Cd 2+ , mostly through plantderived food that has reached the threshold for adverse health effects, and therefore, there is a serious demand to lower human Cd 2+ intake by development of low Cd 2+ -accumulating crops [42,43]. In addition to food consumption, medicinal plants, and processed foods, Cd 2+ is naturally stored at high concentrations in cigarettes [42][43][44]. Cadmium accumulation in leaf tissues damages the photosynthetic machinery, reducing photosynthetic activity [45] and increasing reactive oxygen species (ROS) accumulation, resulting in oxidative stress, programmed cell death, and necrosis [43,[46][47][48][49].…”

“…In addition to food consumption, medicinal plants, and processed foods, Cd 2+ is naturally stored at high concentrations in cigarettes [42][43][44]. Cadmium accumulation in leaf tissues damages the photosynthetic machinery, reducing photosynthetic activity [45] and increasing reactive oxygen species (ROS) accumulation, resulting in oxidative stress, programmed cell death, and necrosis [43,[46][47][48][49].…”

Vacuolar Processing Enzymes in Plant Programmed Cell Death and Autophagy

“…Primarily, it has been found that VPEs are responsible for the maturation of seed storage proteins such as 2S albumin and 12S globulin [ 20 ]. Now it is known that they participate in other developmental processes [ 21 , 22 , 23 , 24 , 25 , 26 ], senescence [ 27 , 28 , 29 ], and environmental stress responses [ 28 , 30 , 31 , 32 ]. During development, senescence, and plant responses to environmental stimuli, both autophagy [ 11 ] and PCD can be initiated [ 33 ].…”

Cell Death Signaling From Endoplasmic Reticulum Stress: Plant-Specific and Conserved Features

“…While the pro-survival function of NRPs culminates with inhibition of cell death-related metacaspases under ER stress conditions, the pro-death function of NRP1 has been linked to the induction of the ANAC036-VPE signaling module (Reis et al, 2016;Yang et al, 2021). More recently, a Cd 2+ -mediated cell death response was associated with induction of both ER stress and the NRPs-GmNACs-VPE signaling module in soybean at the vegetative and reproductive developmental stages (Quadros et al, 2021). Nevertheless, the ER stress-mediated activation of the NRPs-GmNACs-VPE signaling module has not been investigated in soybean seedlings or during germination, and the possibility that NRPs activate specific signaling modules under differential developmental programs remains enigmatic.…”