Plant Cell Advance Online Publication
Published on September 6, 2002; 10.1105/tpc.003285
Received March 22, 2002
Accepted June 26, 2002
Spatiotemporal Patterning of Reactive Oxygen Production and Ca2+ Wave
Propagation in Fucus Rhizoid Cells
Susana M. Coelho 1, Alison R. Taylor 2, Keith P. Ryan 2, Isabel Sousa-Pinto 3, Murray T. Brown 4, and Colin Brownlee 2*
1
Marine Biological Association of the United Kingdom, Citadel Hill, PL1 2PB Plymouth,
United Kingdom; Department of Biological Sciences, University of Plymouth, Drake
Circus, PL4 8AA Plymouth, United Kingdom
2
Marine Biological Association of the United Kingdom, Citadel Hill, PL1 2PB Plymouth,
United Kingdom
3
Centro Interdisciplinar de Invertigçäo Marinha e Ambiental, Universidade
do Porto, Rua do Campo Alegre, 4100 Porto, Portugal
4
Department of Biological Sciences, University of Plymouth, Drake Circus, PL4 8AA
Plymouth, United Kingdom
* To whom correspondence should be addressed. E-mail: cbr{at}mba.ac.uk.
Both Ca2+ and reactive oxygen species (ROS) play critical signaling roles
in plant responses to biotic and abiotic stress. However, the positioning of Ca
2+ 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 H2
O2 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.
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