Below are publications by the group members over the years which are relevant to calcium and calmodulin. Starred publications represent milestones in knowledge. They represent about half the output of the group.
In 1989 the group commenced its most interesting discovery; that is, the use of transgenic aequorin for cytosol calcium measurements. This novel technology has radically changed the perspective of cytosolic calcium in plant cells and has enabled the detection of some 14 different signals which modify cytosolic calcium. Each signal induces calcium transients with different kinetics thus indicating possible specificity in transduction. This new technology has also enabled the construction of plants with aequorin targeted to the chloroplast, nucleus, plasma membrane, rough ER and vacuole membrane. Targeting to guard cells has also been accomplished. Further cell and tissue targeting of aequorin is in progress including pericycle cells, plasmodesmata and nuclear pores. Aequorin has also been introduced into the moss Physcomitrella.
The research now over 15 years has generated much new understanding of how plant cells use cytosolic and organelle calcium to regulate metabolism and development. It has enabled a full comparison to be made between signals which increase calcium in mosses and in higher plants. It has shown how calcium signals are circumstance dependent, changing as the tissue develops or incubation or environmental conditions change. It has shown that signals have a spatial specificity; the combination of organelles and cytoplasm which are mobilised by any one signal is usually unique to that signal. It has shown that gene expression may regulated by cytosolic and nuclear pathways with discrete developmental and spatial changes in calmodulin in both Fucus zygotes and root tissues. It has shown that the calcium system possesses a memory, that there is individuality in response between individual cells and between tissues and plants. It has shown that calcium waves move across tissues and across individual cells. It has shown that single cells can be imaged using luminescence cameras. It has also shown that stochastic resonance might be applicable to calcium signalling, a phenomenon which might account for very sensitive responses to blue light and gravity.
The theme of research amongst group members hinges naturally around calcium and calmodulin and the associated regulation systems although preliminary research is being made to exploit the experience gained in calcium measurements to develop new technologies for measuring other critical molecules.
Below are publications by the group members over the years which
are relevant to calcium and calmodulin. Starred publications represent
milestones in knowledge. They represent about half the output of the group.
Allan, A.C., Fricker,
M.D., Ward, J.L., Beale, M.H. and Trewavas, A.J. (1994). Two transduction
pathways mediate rapid effects of abscisic acid in Commelina guard cells.
Plant Cell 6; 1319-1328.
Collinge, M. and
Trewavas, A.J. (1989). Location of calmodulin in the pea plasma membrane.
J. Biol. Chem. 364, 8865-8872.
Fallon, K., Shacklock,
P. and Trewavas, A.J. (1992) Detection in vivo of very rapid red light-induced
calcium sensitive phosphorylation in etiolated wheat leaf protoplasts.
Plant Physiol. 101, 1039-1045.
Franklin-Tong, V.E.,
Drobak B.K., Allan A.C., Watkins, P.A.C. and Trewavas, A.J. (1996). Growth
of pollen tubes of Papaver rhoeas is regulated by a slow moving calcium
wave propagated by inositol 1,4,5-triphosphate. Plant Cell 8; 1305-1321.
Franklin-Tong, V.E.,
Ride, J.P., Read, N.D., Trewavas, A.J. and Franklin, F.C.H. (1992) The
self-incompatability response in Papaver Rhoeas is mediated by cytosolic
free calcium. Plant Journal 4, 163-177.
Gilroy, S., Fricker,
M., Read, N. and Trewavas, A.J. (1991). Role of calcium in signal transduction
of Commelina guard cells. Plant Cell 3, 333-344.
Gilroy, S., Hughes,
W.A. and Trewavas, A.J. (1986). The measurement of intracellular
calcium levels in protoplasts from higher plant cells. FEBS
Letters, Vol. 199, No. 2, pp. 217-221.
Gilroy, S., Read,
N. and Trewavas, A.J. (1990). Elevation of stomatal cytosol calcium
caged probes initiates stomatal closure. Nature 346, 769-771.
Haley, A., Russell,
A.,Wood, N., Allan, A., Knight, M.R. Campbell, A.K.C and Trewavas, A.J.
. (1995). Mechanical effects on cytoplasmic calcium. Proc.
Nat. Acad. Sci. USA. 92, 4124-4128.
Johnson, C., Knight,
M.R., Kondo T., Masson P., Sedbrook, J., Haley, A. and Trewavas, A.J. (1995).
Circadian oscillations in cytosolic and chloroplastic free calcium in transgenic
luminous plants. Science 269: 1863-1866
Knight, H. Trewavas,
A.J. and Knight M. (1996) Cold calcium signalling in Arabidopsis involves
two cellular pools and a change in calium signature after acclimation.
Plant Cell 8, 489-503.
Knight, M.C., Campbell,
A.K., Smith, S.M. and Trewavas, A.J. (1991). Transgenic plant aequorin
reports the effect of touch and cold shock and elicitors on cytoplasmic
calcium. Nature 352, 524-526.
Knight, M.R., Smith,
S.M. and Trewavas, A.J. (1992) Wind-induced plant motion immediately increases
cytosolic calcium. Proc. Nat. Acad.Sci.USA 89, 4967-4972.
Love, J., Brownlee,
C., and Trewavas, A.J. (1997). Polarized distribution of calmodulin
during zygote development in Fucus. Plant Physiology 115, 249-261.
Malho, R. and Trewavas,
A.J. (1996) Localised apical increases of cytosolic free calcium
controls pollen tube orientation. Plant Cell 8; 1935-1949.
Malho, R. Read,
N.D. Trewavas, A.J.and Pais, S. (1995). Calcium channel activity during
pollen tube growth and reorientation. Plant Cell 7 :1173-1184
Malho, R., Read,
N.D. Pais, S., and Trewavas, A.J. (1993) Role of cytosolic
free calcium inthe reorientation of pollen tube growth. Plant Journal 5,
331-341.
Price, A., Taylor,
A. Ripley, S., Griffiths, A .Trewavas, A.J. Knight, M.R. (1994).
Oxidative signals in tobacco increase cytosolic calcium. Plant Cell
6, 1301-1310.
Russell, A.J., Knight,
M.R., Cove, D.J., Knight, C.D. Trewavas, A.J. and Wang, T.L. (1996).
The moss Physcomitrella transformed with apoaequorin cDNA responds to cold
shock, mechanical perturbation and pH treatment with transient increases
in cytoplasmic calcium. Transgenic Res. 5; 167-170.
Sedbrook, J.C.,
Kronebusch, P.J., Borisy, G.G. Trewavas, A.J. and Masson P.H. (1996) Transgenic
aequorin reveals organ specific cytoslic calium responses to anoxia in
Arabidopsis thaliana seedlings. Plant Physiology, 111; 243-257.
Shacklock, P., Read,
N.D. and Trewavas, A.J. (1992) Cytosolic free calcium mediates red light-induced
photomorphogenesis. Nature 358, 753-755.
Wadkins, J. Knight,
M.R. Trewavas, A.J. and Campbell, A.K.(1994). Chemotactic repellents increase
cytosolic calcium in motile E.coli. Biochem. J. 306, 865-869.
Allan, A., Ward, J., Beale, M and Trewavas, A.J. (1997). The
use of caged hormones in plant cells. Methods in Enzymol. in
press.
Allan, A.C. and Trewavas A.J. (1994). Abscisic acid and gibberellin
perception;inside or out? Plant Physiol. 104, 1107-1108.
Allan, E. and Trewavas, A.J. (1985). Quantitative changes in
calmodulin and NAD kinase during early cell development in the root apex
of Pisum sativum. Planta 165, 493-501.
Allan, E.E.F. and Trewavas, A.J. (1985). Distribution of calmodulin-dependent
and calmodulin-independent NAD kinase during early cell development in
the root apex of Pisum sativum. In Molecular and Cellular Aspects
of Calcium in Plant Development (ed. A.J. Trewavas), pp. 357-358.
Plenum Press, New York and London.
Allan, E.E.F. and Trewavas, A.J. (1985). The concentration of
calmodulin alters during early stages of cell development in the root apex
of Pisum sativum. In Molecular and Cellular Aspects of Calcium in
Plant Development (ed. A.J. Trewavas), pp. 311-312. Plenum Press,
New York and London.
Allan, E.F. and Trewavas, A.J. (1986). Tissue dependent heterogeneity
of cell growth in the root apex of Pisum sativum. Botanical Gazette
147, 258-269.
Allan, E.F. and Trewavas, A.J. (1988). The role of calcium in
metabolic control. In The Biochemistry of Plants (ed. D.D. Davies),
12, 117-153. Academic Press.
Blowers, D. and Trewavas, A.J. (1985). Tyrosine specific protein
kinases in plant tissues. In Molecular and Cellular Aspects of Calcium
in Plant Development (ed. A.J. Trewavas), pp. 339-340. Plenum Press,
New York and London.
Blowers, D., Collinge, M., Gilroy, S., Harvey, H. and Trewavas, A.J.
(1987). Regulation of and by calcium in plants with particular respect
to membranes. A report on progress. In Plant Membranes, Structure
and Function Biogenesis (eds. C.J. Leaver and H. Sze), pp. 371-381.
A.R. Liss.
Blowers, D.P. and Trewavas, A.J. (1987). Autophosphorylation
of plasma membrane bound calcium calmodulin dependent protein kinase from
pea seedlings. Biochemical Biophysical Research Communications
143, 691-696.
Blowers, D.P. and Trewavas, A.J. (1988). Second messengers: their
existence and relationship to protein kinases. In Second Messengers
in Plant Growth and Development (eds. W. Boss and J. Morre), pp.
1-29. Liss, New York.
Blowers, D.P. and Trewavas, A.J. (1988). Phosphatidylinositol kinase
associated with a highly purified protein kinase. FEBS Lett. 238,
87-89.
Blowers, D.P. and Trewavas, A.J. (1989). Autophosphorylation
of phosphoprotein l8(pp18) a calcium and calmodulin regulated plasma membrane
located protein kinase from pea seedlings is a very rapid cycling
of phosphate on serine residues. Plant Physiol. 90, 1279-1285.
Blowers, D.P., Boss, W.F. and Trewavas, A.J. (1988). Rapid changes
in plasma membrane protein phosphorylation during initiation of cell wall
digestion. Plant Physiol. 86, 505-509.
Blowers, D.P., Hetherington, A. and Trewavas, A.J. (1985). Isolation
of plasma-membrane-bound calcium/calmodulin-regulated protein kinase from
pea using Western blotting. Planta 166, 208-215.
Bradford, K. J. and Trewavas, A.J. (1994) Sensitivity thresholds and
variable time scales in plant hormone action. Plant Physiol. 105;
1029-1036.
Campbell, A.K., Trewavas, A.J. and Knight M.R. (1996) Calcium imaging
shows differential senstivity to cooling and communication in luminous
plants. Cell Calcium 19,211-218.
Chiatante, D. Crosti, M., Brusa, P. Trewavas, A.J. John, P. (1993)
Protein kinases and p34 cdc-like protein in root meristem of pea.
Plant Science. 89, 13-21.
Chicester. pp528-532.
Drakeford, D. and Trewavas, A.J. (1985). Binding of verapamil
to maize root membranes. In Molecular and Cellular Aspects of Calcium
in Plant Development (ed. A.J. Trewavas), pp. 423-424. Plenum Press,
New York and London.
Eidne, K.A., Zabavnik, W.T., Allan G., Trewavas, A.J. Read, N.D. and
Anderson, L.J. (1994) Calcium waves and dynamics visualised by confocal
microscopy in Xenopus oocytes expressing cloned TRH receptors. J. Neuroendocrinol.
6, 173-178.
Fallon, K. and Trewavas, A.J. (1994) Phosphorylation of a renatured
protein from etiolated wheat leaf protoplasts is modulated by blue and
red light. Plant Physiol.,105, 253-258.
Fallon, K.M.-and Trewavas, A.J. (1993). The significance of post
translational modification of proteins by phosphorylation in the regulation
of plant development SEB seminar series (ed. N.A.Battey, H.G. Dickinson
and A.N. Hetherington. CUP pp 53-64.
Fricker, M. Gilroy, S. and Trewavas, A.J. (1989). Signal transduction
in plant cells and the calcium message. In Signal Perception and
Transduction in Plant Cells (eds. R. Ranjeva and A. Boudet), pp. 89-102.
Springer-Verlag, Berlin.
Fricker, M.D., Gilroy, S., Read, N.D. and Trewavas, A.J. (1990).
Visualisation and measurement of the calcium message in guard cells.
In Molecular Biology of plant Development S.E.B. Symp. (ed. G. Jenkins
and W. Schuch)., pp 177-190.CUP
Gilroy, S. and Trewavas, A.J. (1990). Signal sensing and signal
transduction across the plasma membrane. In The Plant Plasma Membrane
(eds. I. Moller and C. Larsson), pp. 203-232. Springer-Verlag, Berlin.
Gilroy, S. and Trewavas, A.J. (1994) A decade of plant signals. Bioessays
16; 677-682.
Gilroy, S. Fricker, M., Blowers, D., Harvey, H. Collinge, M. and Trewavas,
A.J. (1989). Calcium channels cytosol calcium and plasma membrane
phosphorylation. An integrated calcium stat system. In Plant
Membrane Transport: The current position (eds. J. Dainty, M. de Michelis,
E. Marre and F. Rasi-Caldogno), pp. 215-225. Elsevier, Amsterdam.
Gilroy, S., Blowers, D.P. and Trewavas, A.J. (1987). Calcium:
a regulation system emerges in plant cells. Development 100, 181-184.
Gilroy, S., Collinge, M., Harvey, H., Blowers, D. and Trewavas, A.J.
(1988). Membranes, Ca2+ and calmodulin. In Plant Membrane Structure
Assembly and Function (eds. J. Harwood and T.J. Walton). Phytochem.
Soc. Europe, pp. 231-237.
Gilroy, S., Fricker, M.D., Read, N. and Trewavas, A.J. (1990).
Fluorescence ratio imaging and photometry of calcium in living plant cells.
Trans. Roy. Microscop. Soc. 1, 475-478.
Gilroy, S., Fricker, M.D., Read, N.D. and Trewavas, A.J. (1992).
The role of Ca2+ and ABA in the regulation of stomatal aperture.
Progress in Plant Growth Regulation. (eds. C.M.Karssen, L.C. Van
Loon and D. Vreugdenhill), pp 105-116. Kluwer, Dordrecht.
Gilroy, S., Hughes, W. and Trewavas, A.J. (1985). Some practical
aspects of the application of Quin-2 to plant systems. In Molecular
and Cellular Aspects of Calcium in Plant Development (ed. A.J. Trewavas),
pp. 373-374. Plenum Press, New York and London.
Gilroy, S., Hughes, W.A. and Trewavas, A.J. (1987). Calmodulin
antagonists increase free cytosolic calcium levels in plant protoplasts
'in vivo'. FEBS Letters 213, 133-137.
Gilroy, S., Hughes, W.A. and Trewavas, A.J. (1989). A comparison
between Quin 2 and aequorin as indicators of cytoplasmic calcium level
in higher plant cell protoplasts. Plant Physiol. 90, 482-491.
Gomez-Lim, M.A., Kelly, P., Sexton, R. and Trewavas, A.J. (1987). Identification
of chitinase mRNA in abscission zones from bean during ethylene induced
abscission. Plant, Cell & Environ. 10, 741-746.
Gong, M, Van Der Luit, A. Knight M.R. and Trewavas, A.J. (1996) Heat
Shock induced change of intracellular calcium level in transgenic tobaco
seedlings. Plant Physiology in press ( January 1998).
Graham, B.M., Blowers, D.P., Trewavas, A.J. and Smith, J.A.C. (1989).
Calcium dependent phosphorylation of tonoplast proteins in the CAM plant
Kalanchoe. In Plant Membrane Transport (eds. J. Dainty, M. de Michelis,
E.Marre and F. Rasi Caldogno. pp. 283-284. Elsevier, Amsterdam.
Harvey, H., Venis, M.A. and Trewavas, A.J. (1989). Partial purification
of a protein from maize coleoptiles membranes binding the calcium channel
antagonist verapamil. Biochem. J., 257, 95-100.
Harvey, H.J., Venis, M.A. and Trewavas, A.J. (1989). The
detection and purification of a verapamil binding protein from plant tissue.
Annals N.Y. Acad. Sci. 560, 50-51.
Hetherington, A.M. and Trewavas, A.J. (1984). The regulation
of membrane-bound protein kinases by phospholipid and calcium. Membranes
and Compartmentation in the Regulation of Plant Functions (ed. A.M.
Boudet), pp. 181-195. Oxford, Clarendon Press. Ann. Proc. Phytochem.
Soc. of Europe 24.
Hetherington, A.M., Blowers, D. and Trewavas, A.J. (1985). Calcium/calmodulin
dependent membrane bound protein kinase. In Molecular and Cellular
Aspects of Calcium in Plant Development (ed. A.J. Trewavas), pp. 123-130.
Plenum Press, New York and London.
Hodick, D., Gilroy, S., Fricker, M. and Trewavas, A.J. (1990).
Cytosolic Ca2+ concentrations and distributions in the strictly tip growing
rhizoids of Chara determined with Indo-1. Botanica Acta 104, 222-229.
Knight H., N.J.Watkins, A.K.Campbell, A.J.Trewavas, M.R.Knight.
1995. luminescent signals in plants.In. Bioluminescence and Chemiluminescence
(eds A.K.Campbell, L.J.Kricka and P.E.Stanley) John Wiley, Chicester.
pp 97-101.
Knight, H., Read, N.D. and Trewavas, A.J. (1993) Confocal microscopy
of living fungal hyphae loaded with Ca sensitive fluorescent dyes.
Mycol. Res., 97, 1505-1515.
Knight, H., Trewavas, A.J. and Knight, M.R. (1997). Calcium signalling
in Arabidopsis thaliana responding to drought and salinity. Plant
J. in press.
Knight, M., Campbell, A., Smith, S. and Trewavas, A.J. (1991).
Reconstituted aequorin in E. coli reports cytoplasmic calcium. FEBS
Lett. 282, 405-408.
Knight, M.R., Read, N.D., Campbell, A.K. and Trewavas, A.J. (1992)
Imaging calcium dynamics in living plants using semi-synthetic recombinant
aequorins. J.Cell Biol. 121,83-90.
Messiaen, J., Read, N.D., Van Cutsem, P. and Trewavas, A.J. (1993).
Cell wall oligogalacturonides increase cytosol calcium in carrot cells.
J. Cell Sci.,104, 365-371 .
Read, N.D., Allan, W.G.T., Knight, M.R., Mahlo, R., Russell, A., Shacklock,,
P. and Trewavas, A.J. (1992). Imaging and measurement of cytosolic
calcium in plant and fungal cells. J. Microscop., 166, 57-86.
Read, N.D., Kellock, L.J., Knight, P.M. and Trewavas, A.J. (1992).
Contact sensing during infection by fungal pathogens. In Perspectives
in Plant Cell Recognition. (eds. J. Callow and J.R.Green). pp 137-173.
CUP
Read, N.D., Knight, H. and Trewavas, A.J. (1992) Fluorescence
ratio imaging and confocal microscopy of calcium in filamentous fungi.
Binary 4, 50-52.
Read, N.D., Shacklock, P.S., Knight, M.R. and Trewavas, A.J. (1993).
Imaging calcium dynamics in living plant cells and tissues. Cell
Biology International, 17, 111-125.
Sinclair, W. and Trewavas, A.J. (1997). Calcium in gravitropism. A
reexamination. Planta 203, 85-91..
Sinclair, W.E., Oliver, I., Maher, P.E. and Trewavas A.J. (1996)
The role of calmodulin in the gravitropic responses of agravitropic mutants
of Arabidopsis thalinana. Planta 199, 343-351.
Takahasi, K., Isobe, M., Knight, M.R., Trewavas, A.J. and Muto, S.
Hypoosmotic shock induces increases in cytosolic free calcium in tobacco
suspension culture cells. Plant Physiology 113: 587-594.
Trewavas, A.J (1983). Nitrate as a plant hormone. British
Plant Growth Regulator Group Monograph 9 (ed. M.B. Jackson), pp. 97-110.
Trewavas, A.J. (1976). Post-translational modification of proteins
by phosphorylation. Ann. Rev. Plant Physiol. 27, 349-376.
Trewavas, A.J. (1985). Growth substances, calcium and the regulation
of cell division. In The Cell Division Cycle in Plants (eds. J.A.
Bryant and D. Francis), pp. 133-156.
Trewavas, A.J. (1985). Molecular and Cellular Aspects of Calcium
in Plant Development. Ed. A.J. Trewavas. Plenum Press,
New York and London.
Trewavas, A.J. (1986). Resource allocation under poor growth
conditions. A major role for growth substances in developmental plasticity.
In Plasticity in Plants (eds. D.H. Jennings and A.J. Trewavas), pp. 31-76.
Trewavas, A.J. and Blowers, D.P. (1990). Protein kinase in the
plant plasma membrane. In Current Topics in Plant Biochemistry and
Physiology, Vol. 9. Plant Protein Phosphorylation. Calcium
and Calmodulin (eds. D.D. Randall and D.G. Blevins), pp. 153-164.
University of Missouri Press.
Trewavas, A.J. and Gilroy, S. (1991). Signal transduction in
plant cells. Trends in Genetics, 7, 356-361.
Trewavas, A.J. and Hetherington, A. (1984). Binding of the specific
calcium channel blocker nitrendipine to pea shoot membranes. Plant
Science Letters 35, 109-113.
Trewavas, A.J. and Hetherington, A. (1984). Regulation of a membrane
bound protein kinase in pea shoots by calcium ions. Planta 161, 409-418.
Trewavas, A.J. and Knight, M.R. (1992) The regulation of shape
and form by cytosol calcium. In Shape and form in plant
and fungal cells. (eds. D.Ingram and A.Hudson) pp 221-233. Acad. Press
London.
Trewavas, A.J. and Knight, M.R. (1994). Mechanical signalling, calcium
and plant form. Plant Mol. Biol. 26, 1329-1341.
Trewavas, A.J. and Malho, R. (1997). Signal transduction and perception:
the origin of the phenotype. Plant Cell 9, 1181-1195.
Trewavas, A.J. and Smart, C.C. (1984). Abscisic acid-induced
turion formation in Spirodela polyrrhiza. IV. Comparative ion flux
characteristics of the turion and the vegetative frond and the effect of
ABA during early turion development. Plant, Cell and Environment
7, 521-531.
Trewavas, A.J. and Stratton, B.R. (1981). Phosphorylation of
histone Hl during the cell cycle of artichoke. Plant, Cell and Environment
4, 419-427.
Trewavas, A.J. Campbell, A.K. and Knight M.R. 1996. Compartmentalisation
of calcium in plant cells. Biochem Soc Transactions 24; 971-974.
Trewavas, A.J. Read, N.D. and Knight, M.R. (1992) Calcium
measurement and dynamics during signal transduction in living plant cells.
In Biochemical mechanisms involved in growth regulation. (eds. D.Chiatante,
J.Gallon, C.J.Smith, and G. Zocchi) pp217-231. OUP
Trewavas, A.J., Sexton, R. and Kelly, P. (1984). Polarity, calcium
and abscission: molecular bases for developmental plasticity in plants.
Journal of Embryology and Experimental Morphology 83, 179-195.
Watkins, N.J., M.R.Knight, A.J.Trewavas, Campbell. 1995 Engineering
aequorin as an intracellular calcium indicator in Escherichia coli and
plants. In. Bioluminescnece and Chemiluminescence. (eds A.K.Campbell
L.J.Kricka and P.E.Stanley) John Wiley,