Abstract

Calcium is used by plants as an intracellular messenger in the detection of and response to a plethora of environmental stimuli and contributes to a fine-tuned internal regulation. Interest in the role of different subcellular compartments in Ca(2+) homeostasis and signalling has been growing in recent years. This work has evaluated the potential participation of non-green plastids and chloroplasts in the plant Ca(2+) signalling network using heterotrophic and autotrophic cell suspension cultures from Arabidopsis thaliana plant lines stably expressing the bioluminescent Ca(2+) reporter aequorin targeted to the plastid stroma. Our results indicate that both amyloplasts and chloroplasts are involved in transient Ca(2+) increases in the plastid stroma induced by several environmental stimuli, suggesting that these two functional types of plastids are endowed with similar mechanisms for handling Ca(2+) A comparison of the Ca(2+) trace kinetics recorded in parallel in the plastid stroma, the surface of the outer membrane of the plastid envelope, and the cytosol indicated that plastids play an essential role in switching off different cytosolic Ca(2+) signals. Interestingly, a transient stromal Ca(2+) signal in response to the light-to-dark transition was observed in chloroplasts, but not amyloplasts. Moreover, significant differences in the amplitude of specific plastidial Ca(2+) changes emerged when the photosynthetic metabolism of chloroplasts was reactivated by light. In summary, our work highlights differences between non-green plastids and chloroplasts in terms of Ca(2+) dynamics in response to environmental stimuli.

Highlights

  • In plants Ca2+ is used as an intracellular messenger to transduce a plethora of abiotic and biotic stimuli

  • Our results indicate that both amyloplasts and chloroplasts are involved in transient Ca2+ increases in the plastid stroma induced by several environmental stimuli, suggesting that these two functional types of plastids are endowed with similar mechanisms for handling Ca2+

  • To dissect the involvement of chloroplasts and non-green plastids in Ca2+ handling during signal transduction events, we monitored changes in [Ca2+] in response to different environmental stimuli in A. thaliana heterotrophic and autotrophic cell suspension cultures stably expressing aequorin targeted to the organelle stroma

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Summary

Introduction

In plants Ca2+ is used as an intracellular messenger to transduce a plethora of abiotic and biotic stimuli. A wide array of environmental stimuli have been shown to evoke specific intracellular spatio-temporal Ca2+ signals, which are further transduced by Ca2+ sensor proteins into transcriptional and metabolic responses (Dodd et al, 2010; Whalley and Knight, 2013). Research on the intracellular compartmentalization of the ion has so far mainly focused on the vacuole, which is considered to be the major Ca2+ storage compartment in the plant cell, and for which extensive knowledge about Ca2+ transporters localized at the tonoplast is already available (Peiter, 2011; Martinoia et al, 2012; Xu et al, 2015). The role of Ca2+ in chloroplasts, and in plastids in general, is still elusive, with only little information so far available on the involvement of plastids in Ca2+ homeostasis and the generation of specific Ca2+ signals inside the plastids (Nomura and Shiina, 2014). It has to be considered that different functional types of plastids are present in plants, and their structural and physiological differences may lead to differential involvement in the Ca2+ signalling network

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