First published online September 6, 2002; 10.1105/tpc.003285
The Plant Cell, Vol. 14, 2369-2381,
October 2002, Copyright © 2002,
American Society of Plant Biologists
Spatiotemporal Patterning of Reactive Oxygen Production and Ca2+ Wave Propagation in Fucus Rhizoid Cells
Susana M. Coelhoa,b,
Alison R. Taylora,
Keith P. Ryana,
Isabel Sousa-Pintoc,
Murray T. Brownb and
Colin Brownlee1,a
a Marine Biological Association of the United Kingdom, Citadel Hill, PL1 2PB Plymouth, United Kingdom
b Department of Biological Sciences, University of Plymouth, Drake Circus, PL4 8AA Plymouth, United Kingdom
c Centro Interdisciplinar de Investigação Marinha e Ambiental, Universidade do Porto, Rua do Campo Alegre, 4100 Porto, Portugal
1 To whom correspondence should be addressed. E-mail cbr{at}mba.ac.uk; fax 01752633102
Both Ca2+ and reactive oxygen species (ROS) play critical signaling roles in plant responses to biotic and abiotic stress. However, the positioning of Ca2+ and ROS (in particular H2O2) after a stress stimulus and their subcellular interactions are poorly understood. Moreover, although information can be encoded in different patterns of cellular Ca2+ signals, little is known about the subcellular spatiotemporal patterns of ROS production or their significance for downstream responses. Here, we show that ROS production in response to hyperosmotic stress in embryonic cells of the alga Fucus serratus consists of two distinct components. The first ROS component coincides closely with the origin of a Ca2+ wave in the peripheral cytosol at the growing cell apex, has an extracellular origin, and is necessary for the Ca2+ wave. Patch-clamp experiments show that a nonselective cation channel is stimulated by H2O2 and may underlie the initial cytosolic Ca2+ increase. Thus, the spatiotemporal pattern of the Ca2+ wave is determined by peripheral ROS production. The second, later ROS component localizes to the mitochondria and is a direct consequence of the Ca2+ wave. The first component, but not the second, is required for short-term adaptation to hyperosmotic stress. Our results highlight the role of ROS in the patterning of a Ca2+ signal in addition to its function in regulating cell wall strength in the Fucus embryo.
This article has been cited by other articles:
|
|
|
|
 
J.-H. Li, Y.-Q. Liu, P. Lu, H.-F. Lin, Y. Bai, X.-C. Wang, and Y.-L. Chen
A Signaling Pathway Linking Nitric Oxide Production to Heterotrimeric G Protein and Hydrogen Peroxide Regulates Extracellular Calmodulin Induction of Stomatal Closure in Arabidopsis
Plant Physiology,
May 1, 2009;
150(1):
114 - 124.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Xue, X. Li, W. Zhu, C. Wu, G. Yang, and C. Zheng
Cotton metallothionein GhMT3a, a reactive oxygen species scavenger, increased tolerance against abiotic stress in transgenic tobacco and yeast
J. Exp. Bot.,
January 1, 2009;
60(1):
339 - 349.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Cardenas, S. T. McKenna, J. G. Kunkel, and P. K. Hepler
NAD(P)H Oscillates in Pollen Tubes and Is Correlated with Tip Growth
Plant Physiology,
December 1, 2006;
142(4):
1460 - 1468.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Camello-Almaraz, P. J. Gomez-Pinilla, M. J. Pozo, and P. J. Camello
Mitochondrial reactive oxygen species and Ca2+ signaling
Am J Physiol Cell Physiol,
November 1, 2006;
291(5):
C1082 - C1088.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. S. Terada
Specificity in reactive oxidant signaling: think globally, act locally
J. Cell Biol.,
August 28, 2006;
174(5):
615 - 623.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. M. Kwak, V. Nguyen, and J. I. Schroeder
The Role of Reactive Oxygen Species in Hormonal Responses
Plant Physiology,
June 1, 2006;
141(2):
323 - 329.
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Weinberger, G. Pohnert, M.-L. Berndt, K. Bouarab, B. Kloareg, and P. Potin
Apoplastic oxidation of L-asparagine is involved in the control of the green algal endophyte Acrochaete operculata Correa & Nielsen by the red seaweed Chondrus crispus Stackhouse
J. Exp. Bot.,
May 1, 2005;
56(415):
1317 - 1326.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y.-L. Chen, R. Huang, Y.-M. Xiao, P. Lu, J. Chen, and X.-C. Wang
Extracellular Calmodulin-Induced Stomatal Closure Is Mediated by Heterotrimeric G Protein and H2O2
Plant Physiology,
December 1, 2004;
136(4):
4096 - 4103.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. C. Mori and J. I. Schroeder
Reactive Oxygen Species Activation of Plant Ca2+ Channels. A Signaling Mechanism in Polar Growth, Hormone Transduction, Stress Signaling, and Hypothetically Mechanotransduction
Plant Physiology,
June 1, 2004;
135(2):
702 - 708.
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Sagi, O. Davydov, S. Orazova, Z. Yesbergenova, R. Ophir, J. W. Stratmann, and R. Fluhr
Plant Respiratory Burst Oxidase Homologs Impinge on Wound Responsiveness and Development in Lycopersicon esculentum
PLANT CELL,
March 1, 2004;
16(3):
616 - 628.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. K.-Y. NG and M. R. MCAINSH
Encoding Specificity in Plant Calcium Signalling: Hot-spotting the Ups and Downs and Waves
Ann. Bot.,
October 1, 2003;
92(4):
477 - 485.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. M. Parton, S. Fischer-Parton, A. J. Trewavas, and M. K. Watahiki
Pollen tubes exhibit regular periodic membrane trafficking events in the absence of apical extension
J. Cell Sci.,
July 1, 2003;
116(13):
2707 - 2719.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Bouche, A. Fait, D. Bouchez, S. G. Moller, and H. Fromm
Mitochondrial succinic-semialdehyde dehydrogenase of the {gamma}-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants
PNAS,
May 27, 2003;
100(11):
6843 - 6848.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
