Insights into Plant Programmed Cell Death Induced by Heavy Metals-Discovering a Terra Incognita.

Klaudia Sychta,Aneta Słomka,Elżbieta Kuta

doi:10.3390/cells10010065

Abstract

Programmed cell death (PCD) is a process that plays a fundamental role in plant development and responses to biotic and abiotic stresses. Knowledge of plant PCD mechanisms is still very scarce and is incomparable to the large number of studies on PCD mechanisms in animals. Quick and accurate assays, e.g., the TUNEL assay, comet assay, and analysis of caspase-like enzyme activity, enable the differentiation of PCD from necrosis. Two main types of plant PCD, developmental (dPCD) regulated by internal factors, and environmental (ePCD) induced by external stimuli, are distinguished based on the differences in the expression of the conserved PCD-inducing genes. Abiotic stress factors, including heavy metals, induce necrosis or ePCD. Heavy metals induce PCD by triggering oxidative stress via reactive oxygen species (ROS) overproduction. ROS that are mainly produced by mitochondria modulate phytotoxicity mechanisms induced by heavy metals. Complex crosstalk between ROS, hormones (ethylene), nitric oxide (NO), and calcium ions evokes PCD, with proteases with caspase-like activity executing PCD in plant cells exposed to heavy metals. This pathway leads to very similar cytological hallmarks of heavy metal induced PCD to PCD induced by other abiotic factors. The forms, hallmarks, mechanisms, and genetic regulation of plant ePCD induced by abiotic stress are reviewed here in detail, with an emphasis on plant cell culture as a suitable model for PCD studies. The similarities and differences between plant and animal PCD are also discussed.

Highlights

Accepted: 30 December 2020Heavy metals are a harsh factor influencing plants that may disturb the biological processes in plant cells
True apoptosis is not observed in plant cells, different abiotic factors cause morphological changes that are very similar to those occurring during animal cell apoptosis in a process called apoptotic-like programmed cell death (PCD) (AL-PCD) (Box 2)
The regulation and execution processes of PCD, the processes induced by abiotic factors such as heavy metals, remain terra incognita (Box 5), some of the biochemical, molecular and morphological mechanisms are known

Summary

Introduction

Heavy metals are a harsh factor influencing plants that may disturb the biological processes in plant cells. Some morphological and biochemical features, such as by chloroplasts along with DEFENDER AGAINST CELL DEATH1 (DAD1) and DAD2, calcium signaling, generation of ROS or induction of VPE activity, are similar in dPCD and regulates OXI1 expression Another way is retrograde signaling pathway mediated by ePCD [29]. High expression of LSD1 may antagonize cell death, whereas LOL1 overexpression will activate PCD [58] Another gene family important in plant PCD activation is Receptor-like/Pelle kinases, among which a group of cysteine-rich Receptor-like/Pelle kinases play important role in PCD caused by environmental stimuli [59,60]. Crosstalk between JA and SA, produced by chloroplasts along with DEFENDER AGAINST CELL DEATH1 (DAD1) and DAD2, regulates OXI1 expression Another way is retrograde signaling pathway mediated by singlet oxygen under light stress. Plant caspase-like proteases, structurally distinct from animal caspases, have similar substrate cleavage specificities [65]

PCD in Plants and Apoptosis in Animals

PCD Induced by Heavy Metals in Plant and Animal Cells

Summary

Vacuolization

Regulation and Execution Processes Engaging Plant Proteases with Caspase-Like

Conclusions and Future Perspectives