Abstract

ABSTRACTWe uncovered that the level of autophagy in plant cells undergoing programmed cell death determines the fate of the surrounding cells. Our approach consisted of using Arabidopsis thaliana cell cultures capable of differentiating into two different cell types: vascular tracheary elements (TEs) that undergo programmed cell death (PCD) and protoplast autolysis, and parenchymatic non-TEs that remain alive. The TE cell type displayed higher levels of autophagy when expression of the TE-specific METACASPASE9 (MC9) was reduced using RNAi (MC9-RNAi). Misregulation of autophagy in the MC9-RNAi TEs coincided with ectopic death of the non-TEs, implying the existence of an autophagy-dependent intercellular signalling from within the TEs towards the non-TEs. Viability of the non-TEs was restored when AUTOPHAGY2 (ATG2) was downregulated specifically in MC9-RNAi TEs, demonstrating the importance of autophagy in the spatial confinement of cell death. Our results suggest that other eukaryotic cells undergoing PCD might also need to tightly regulate their level of autophagy to avoid detrimental consequences for the surrounding cells.

Highlights

  • The development of multicellular organisms involves programmed cell death (PCD)

  • MC9 is involved in tracheary elements (TEs) differentiation in cell cultures We first investigated whether MC9 is expressed in differentiating TEs in vitro as it is in planta (Bollhöner et al, 2013)

  • Consistent with in planta data (Bollhöner et al, 2013), microscopy analysis of three transgenic lines revealed that MC9:GFP was expressed in TEs, recognizable by their patterned secondary cell walls (SCW) (Fig. 1A)

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Summary

Introduction

The development of multicellular organisms involves programmed cell death (PCD). In land plants, PCD – followed by complete cellular autolysis – likely represented the first evolutionary step in the acquisition of specialized water-conducting structures that were necessary for survival in the dry atmosphere (Escamez and Tuominen, 2014; Friedman and Cook, 2000). TE cell death is brought about by rupture of the central vacuole (Burgess and Linstead, 1984; Groover and Jones, 1999; Kuriyama, 1999), which is believed to allow TE autolysis to occur by releasing certain. §Present address: Department of Ecology, Environment and Plant Sciences, Stockholm University, SE-106 91 Stockholm, Sweden. No molecular effectors of TE cell death have been identified, but TE post-mortem autolysis has been shown to involve specific hydrolases (Avci et al, 2008; Ito and Fukuda, 2002) including Arabidopsis thaliana METACASPASE9 (MC9) (Bollhöner et al, 2013)

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