ReviewCalcium: silver bullet in signaling
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.
References (240)
Calcium channels in higher plants
Biochim. Biophys. Acta
(2000)- et al.
Ca2+ signaling in plant cells: the big network!
Curr. Opin. Plant Biol.
(1998) - et al.
Cyclic GMP and calcium mediate phytochrome phototransduction
Cell
(1994) - et al.
Salinity and hyperosmotic stress induce rapid increases in phosphatidylinositol 4,5-bisphosphate, diacylglycerol pyrophosphate, and phosphatidylcholine in Arabidopsis thaliana cells
J. Biol. Chem.
(1999) - et al.
Abscisic acid induces a cytosolic calcium decreases in barley aleurone protoplasts
FEBS Lett.
(1991) - et al.
Calcium imaging shows differential sensitivity to cooling and communication in luminous transgenic plants
Cell Calc.
(1996) - et al.
An increase in cytosolic calcium ion concentration precedes hypoosmotic shock-induced activation of protein kinases in tobacco suspension culture cells
FEBS Lett.
(1997) - et al.
H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response
Cell
(1994) - et al.
Calcium-mediated apoptosis in a plant hypersensitive disease resistance response
Curr. Biol.
(1996) - et al.
Calcium spiking in plant root hairs responding to Rhizobium nodulation signals
Cell
(1996)