Editors' ChoicePlant biology

Ferroptosis-like cell death in plants

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Sci. Signal.  28 Feb 2017:
Vol. 10, Issue 468, eaan0450
DOI: 10.1126/scisignal.aan0450

Heat stress induces a form of cell death in plants that is morphologically and biochemically similar to ferroptosis in animal cells.

Animals exhibit many morphologically and biochemically distinct forms of regulated cell death, such as apoptosis, ferroptosis, and pyroptosis (see Todorov and Linkermann). Plants also undergo distinct types of cell death, though none of these are directly analogous to apoptosis. Distéfano et al. described a regulated response to heat shock in plants that resembles ferroptosis, which in animal cells is defined by its dependence on cellular iron and an accumulation of reactive oxygen species (ROS). Heat shocking Arabidopsis thaliana seedlings at 55°C for 10 min triggers regulated cell death, whereas longer exposure or higher temperatures induces necrosis. When seedlings were pretreated with an iron-chelating compound or with an antioxidant known to inhibit ferroptosis in animals, heat shock at 55°C (but not 77°C) resulted in less cell death in the root hairs than without pretreatment. Neither compound affected developmentally regulated programmed cell death nor cell death caused by treatment with hydrogen peroxide or sodium chloride, suggesting that iron was involved in this specific form of heat stress–induced cell death. Microscopy of root hair cells revealed that the 55°C heat shock, but not exposure to 77°C or to the other stressors, caused cytoplasmic retraction and the formation of lytic vacuoles, a morphological hallmark of regulated cell death in plants. In addition, the root hair cells of heat-shocked plants had shrunken mitochondria, a feature of ferroptosis in animal cells. ROS accumulated in the root hair cells of heat-shocked seedlings and in heat-shocked A. thaliana cultured cells prior to death, and the ferroptosis inhibitors prevented ROS accumulation. Also analogously to ferroptosis in animal cells, preventing peroxidation of polyunsaturated fatty acids inhibited ROS accumulation and prevented cell death after heat shock in both plant roots and in plant cell culture. Root hair cells from heat-shocked seedlings exhibited decreased glutathione concentrations, which were not reversed by treatment with ferroptosis inhibitors, but treatment with glutathione reduced heatshock–induced cell death. Treatment with ferroptosis inhibitors also increased plant survival after exposure to 43°C for an hour, which caused bleaching and death over the course of several days in untreated plants. These observations reveal parallels between mechanisms of regulated cell death in environmentally stressed plants and in animal cells undergoing ferroptosis and suggest that this pathway could be targeted to improve plant heat tolerance.

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