Spermine and spermidine inhibit or induce programmed cell death in Arabidopsis thaliana in vitro and in vivo in a dose‐dependent manner

• Published in: The FEBS journal 2024-08, Vol.291 (16), p.3665-3685
• Main Authors: Burke, Rory, Nicotra, Daniele, Phelan, Jim, Downey, Frances, McCabe, Paul F., Kacprzyk, Joanna
• Format: Article
• Language: English
• Subjects: Apoptosis; Arabidopsis; Arabidopsis cell suspension culture; Arabidopsis thaliana; biochemical compounds; Biomolecules; biotic stress; Cell death; dose response; Gene expression; Mortality; Oxidative stress; pathogens; phenotype; Phenotypes; Plant cells; plant programmed cell death; Polyamines; programmed cell death; root hair assay; Root hairs; Seedlings; Spermidine; Spermine; stress tolerance
• ISSN: 1742-464X; 1742-4658; 1742-4658
• DOI: 10.1111/febs.17165

Polyamines are ubiquitous biomolecules with a number of established functions in eukaryotic cells. In plant cells, polyamines have previously been linked to abiotic and biotic stress tolerance, as well as to the modulation of programmed cell death (PCD), with contrasting reports on their pro‐PCD and pro‐survival effects. Here, we used two well‐established platforms for the study of plant PCD, Arabidopsis thaliana suspension cultures cells and the root hair assay, to examine the roles of the polyamines spermine and spermidine in the regulation of PCD. Using these systems for precise quantification of cell death rates, we demonstrate that both polyamines can trigger PCD when applied exogenously at higher doses, whereas at lower concentrations they inhibit PCD induced by both biotic and abiotic stimuli. Furthermore, we show that concentrations of polyamines resulting in inhibition of PCD generated a transient ROS burst in our experimental system, and activated the expression of oxidative stress‐ and pathogen response‐associated genes. Finally, we examined PCD responses in existing Arabidopsis polyamine synthesis mutants, and identified a subtle PCD phenotype in Arabidopsis seedlings deficient in thermo‐spermine. The presented data show that polyamines can have a role in PCD regulation; however, that role is dose‐dependent and consequently they may act as either inhibitors, or inducers, of PCD in Arabidopsis. Polyamines have previously been linked to modulation of programmed cell death (PCD), but the reports on their pro‐death and pro‐survival effects in plants are frequently contrasting. In this work, we show that exogenous polyamines spermidine and spermine may inhibit or induce PCD in Arabidopsis thaliana in a dose‐dependent manner. This hormetic effect is likely mediated by reactive oxygen species (ROS) generated in response to polyamine supplementation.