Elsevier

Plant Science

Volume 160, Issue 3, 5 February 2001, Pages 381-404
Plant Science

Review
Calcium: silver bullet in signaling

https://doi.org/10.1016/S0168-9452(00)00386-1Get rights and content

Abstract

Accumulating evidence suggests that Ca2+ serves as a messenger in many normal growth and developmental process and in plant responses to biotic and abiotic stresses. Numerous signals have been shown to induce transient elevation of [Ca2+]cyt in plants. Genetic, biochemical, molecular and cell biological approaches in recent years have resulted in significant progress in identifying several Ca2+-sensing proteins in plants and in understanding the function of some of these Ca2+-regulated proteins at the cellular and whole plant level. As more and more Ca2+-sensing proteins are identified it is becoming apparent that plants have several unique Ca2+-sensing proteins and that the downstream components of Ca2+ signaling in plants have novel features and regulatory mechanisms. Although the mechanisms by which Ca2+ regulates diverse biochemical and molecular processes and eventually physiological processes in response to diverse signals are beginning to be understood, recent studies have raised many interesting questions. Despite the fact that Ca2+ sensing proteins are being identified at a rapid pace, progress on the function(s) of many of them is limited. Studies on plant ‘signalome’ — the identification of all signaling components in all messengers mediated transduction pathways, analysis of their function and regulation, and cross talk among these components — should help in understanding the inner workings of plant cell responses to diverse signals. New functional genomics approaches such as reverse genetics, microarray analyses coupled with in vivo protein–protein interaction studies and proteomics should not only permit functional analysis of various components in Ca2+ signaling but also enable identification of a complex network of interactions.

Introduction

Plant growth and development is controlled by hormonal and environmental signals. Plants, unlike animals, are immobile and therefore have developed mechanisms to sense and respond to the biotic and abiotic stresses so that they can better adapt to their environment. How plants sense these various signals and produce an appropriate response has fascinated plant biologists over a century and has become an area of intense investigation in recent years. Research during the last two decades has clearly established that Ca2+ acts as an intracellular messenger in coupling a wide-range of extracellular signals to specific responses. Although Ca2+ is implicated in regulating a number of fundamental cellular processes that are involved in cytoplasmic streaming, thigmotropism, gravitropism, cell division, cell elongation, cell differentiation, cell polarity, photomorphogenesis, plant defense and stress responses, the mechanisms by which Ca2+ controls these processes are only beginning to be understood. Because of the space limitations, my intention here is to summarize recent progress in understanding Ca2+-mediated signal transduction pathways with emphasis on the current status of research, gaps in our knowledge and future directions.

Section snippets

Signals and cytosolic Ca2+

Improved methods to monitor free [Ca2+]cyt levels, especially using transgenic plants expressing Ca2+ reporter proteins, have greatly helped in demonstrating signal-induced changes in free [Ca2+]cyt level [1], [2], [3], [4]. The concentration of Ca2+ in the cytoplasm of plant cells is maintained low in the nanomolar range (100–200 nM) [4], [5]. However, Ca2+ concentration in the cell wall and in organelles is in the millimolar range (Fig. 1) [6], [7]. Despite the existence of a large

Ca2+ sensors

Transient Ca2+ increase in the cytoplasm in response to signals is sensed by an array of Ca2+-sensors (Ca2+-binding proteins) which decode Ca2+ signal. Once Ca2+ sensors decode the elevated [Ca2+]cyt, Ca2+ efflux into the cell exterior and/or sequestration into cellular organelles such as vacuoles, ER and mitochondria restores its levels to resting state. A large number of Ca2+ sensors have been characterized in plants, which can be grouped into four major classes [80], [81]. These include (A)

Ca2+ and gene expression

Although there is a great deal of information on the involvement of Ca2+ in regulating various physiological processes [213], [214], the role of Ca2+ in regulating gene expression in plants is forthcoming only recently. Manipulation of [Ca2+]cyt by various means is shown to affect the expression of specific genes in plants. Mannitol-induced expression of RAB and AtP5CS1 genes is blocked in the presence Ca2+ channel blockers like verapamil or lanthanum or the Ca2+ chelator EGTA [30], [215]. The

Specificity in decoding Ca2+ signal

The fact that Ca2+ is a messenger in transducing a wide range of signals into diverse responses raises an important question — How does Ca2+ achieve specificity in eliciting a response to a given signal? A number of factors are likely to be involved in controlling the specificity. First, competence of an organ, a tissue or a cell type within the tissue to respond to a given stimulus. In vivo imaging of cold-induced changes in [Ca2+]cyt indicate that cotyledons and roots of a seedling are highly

Future directions

During the last decade, significant progress has been made in demonstrating that signals not only elevate [Ca2+]cyt but the Ca2+ signature generated by each signal is likely to be different. Based on what is already known, it is clear that plants contain many unique Ca2+ sensing proteins with novel regulatory mechanisms that have evolved to perform plant-specific functions. It is likely that many more novel Ca2+ sensing proteins will be identified, especially as the Arabidopsis genome sequence

Acknowledgements

I would like to thank Dr Irene Day and Dr Vaka Reddy for critically reading the manuscript; Bryan Criswell for his help in preparing the figures. My apologies to those colleagues in the field whose work was not mentioned due to space limitations. Research on Ca2+ signaling in my laboratory is supported by grants from NSF, Agricultural Experiment Station and NASA.

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