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Plant Physiol, September 2002, Vol. 130, pp. 4-5
NEWS FROM THE ARCHIVES
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Do Plants Have Ouabain (OU)-Sensitive ATPases? |
In the 1960s and 1970s, many plant
physiologists labored under the assumption that any
electrogenic ion pumps discovered in plant cells would be similar, if
not identical, to the electrogenic Na+,
K+-ATPase found in the plasma membrane of animal cells.
These expectations eventually subsided as evidence, now
incontrovertible, mounted that electrogenesis in plants involves
primarily OU-insensitive H+-ATPases. Before this consensus
was reached, however, many biochemical and physiological studies were
performed concerning the effects of OU on plants. Although these
results were not entirely negative, interest in the question of the
mode of action of OU on plants came to a virtual standstill as
researchers focused their attentions on elucidating the properties of
the dominant OU-insensitive H+-ATPases. It is not the
purpose of this review to dispute the fundamental importance of
OU-insensitive H+-ATPases in plant function, but rather to
suggest that there may be some minor ATPases within higher plants that
possess sensitivity to OU.
A survey of the botanical literature has found more than 50 published
reports consistent with the idea that pharmacologically valid
concentrations of OU (i.e. 125 µM or less) have
physiological effects on plants or inhibit plant membrane ATPase
activities in vitro. It is regrettable, therefore, that studies of the
effects of OU on plants virtually ceased in the 1990s, even
though there is now a whole new arsenal of molecular techniques that
could be brought to bear on the question of the sites of OU action in plants. It is hoped that this review will revitalize interest in this
moribund question.
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Origins of OU Sensitivity |
The H+-ATPases of plants and fungi,
the Na+, K+-ATPase of animals, as well as
certain other types of ATPases (e.g. the plasma membrane
Ca2+-ATPase, the gastric H+,
K+-ATPase, and the sarcoplasmic reticulum
Ca2+-ATPase) are all related members of a larger molecular
family the P-type ATPases (Green, 1992 ). The fact that at least one
other P-type ATPase besides the Na+, K+-ATPase
exhibits sensitivity to OU, namely the H+,
K+-ATPase of colonocytes (Cougnon et al., 1996), raises the
possibility that the OU-sensitive ATPases in plants need not
necessarily act as Na+ pumps. Experiments have shown that
there may be less distinction between the various types of P-type
ATPases than their essentialist names would suggest. For example, the
Na+, K+-ATPase of animal cells can, under
certain conditions, pass protons instead of Na+ ions
(Polvani and Blostein, 1988), and, conversely, the gastric H+, K+-ATPase can, under certain conditions,
pass Na+ ions instead of protons (Polvani et al., 1989).
Thus, researchers should be attentive to the possibility
that OU-sensitive ATPases in plants could be serving
slightly or very different functions from their counterparts in
animal cells.
Reports that OU affects physiological processes in ciliates (Fabczak
and Fabczak, 1989), euglenozoa (Mikolajczyk, 1986), fungi (Ayres et
al., 1987; Rauforova et al., 1997), green algae (Meszes and Erdei,
1969), and cyanobacteria (Iwano, 1995) suggest that OU sensitivity may
have had an ancient origin during the molecular phylogeny of P-type ATPases.
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Physiological Effects of OU |
OU has been found to influence many physiological processes
and parameters in plants, including membrane potential (Stolarek, 1968a; Latala, 1975; Zientara, 1983; Solic and Zuvic, 1990),
Na+ fluxes (Cram, 1968; Ozerskii, 1969; Davis
and Jaworski, 1979), K+ fluxes (MacRobbie, 1962; Stolarek,
1968b), amino acid uptake (Basu et al., 1988), electrical signaling
(Desbiez, 1973; Pazurkiewicz-Kocot and Stolarek, 1980; Karege et
al., 1982; Slesak, 1984), stomatal aperture (Thomas, 1970; Turner,
1973), pulvinar function (Watanabe, 1971; Jonas, 1976) respiration
(Legros et al., 1973; Migliaccio 1973) secretion (Brown et al., 1964),
root pressure (Mozhaeva et al., 1979), transpiration (Morant-Avice et
al., 1997), and flowering (Oota, 1974).
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Two OU-Sensitive ATPases? |
Two studies (Brown et al., 1964; Thomas, 1970)
produced OU dose response curves very similar to those
commonly found in animal studies. In other cases (e.g. Nassery and
Baker, 1972), the dose response curves for OU sensitivity are shifted
over more than 3 orders of magnitude. This suggests that there are may
be two OU-sensitive processes in plants: one (type 1) with an
I50 of approximately 0.1 µM, and the
other (type 2) with a concentration for half-inhibition
(I50) of approximately 100 µM. Oota's (1974) finding of an unusual U-shaped dose response curve suggests that the
Lemna gibba flowering response he studied may be lowered
by type 1 OU inhibition and enhanced by type 2 OU inhibition.
Other evidence that there may be more than one site of OU sensitivity
in plants comes from biochemical studies. Lindberg (1982) concluded
that two forms of OU-sensitive ATPases exist in sugar beet (Beta
vulgaris) roots; one with an optimal pH of 5.5 to 6.0, and the
other with an optimal pH of 8.0. It has been hypothesized that the
acidophilic OU-sensitive ATPase is endomembranous. It may be germane in
this regard that plants do have a P-type Ca2+-ATPase coded
for by a single gene, which is found in both the plasma membrane and
the vacuolar membrane (Ferrol and Bennett, 1996). Because OU interacts
with the extracellular face of the Na+,
K+-ATPase, researchers have tended to ignore the effects of
intracellular OU. OU, however, is also taken up internally
into animal cells (Nunez-Duran et al., 1988). The possibility that OU
may have an intracellular site of action in plants is one that should
be considered.
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FOOTNOTES |
www.plantphysiol.org/cgi/doi/10.1104/pp.900046.
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LITERATURE CITED |
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(1987)
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Involvement of phytochrome in calcium-dependent, calmodulin-independent L-leucine uptake in Brassica.
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Cougnon M, Planelles G, Crowson MS, Shull GE, Rossier BC, Juisser R
(1996)
The rat distal colon P-ATPase
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J Biol Chem
271: 7277-7280[Abstract/Free Full Text] -
Cram WJ
(1968)
The effects of ouabain on sodium and potassium fluxes in excised roots of carrot.
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Davis RF, Jaworski AZ
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Modulators of intracellular sodium concentration affect contractile vacuole activity in ciliate Blepharisma japonicum.
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(1976)
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(1975)
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(1982)
Sucrose and ouabain effects on the kinetic properties of a membrane bound (Na+ + K+ + Mg2+) ATPase in sugar beet roots.
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Ouabain uptake by endocytosis in isolated guinea pig atria.
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Peter V. Minorsky
Department of Natural Sciences
Mercy College
Dobbs Ferry, NY 10522
© 2002 American Society of Plant Physiologists
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Do Plants Have Ouabain...
Origins of OU Sensitivity