Flux Control in Biological Systems. From Enzymes to Populations and Ecosystems

498 Pages·1994·13.49 MB·English

by  Ernst-Detlef Schulze (Auth.)

Physiological Ecology
A Series of Monographs, Texts, and Treatises
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Fakhri Bazzaz F. Stuart Chapin James R. Ehleringer
Robert W. Pearcy Martyn M. Caldwell E.-D. Schulze
T. T. KOZLOWSKI (Ed.). Growth and Development of Trees, Vol-
umes I and II, 1971
D. HILLEL (Ed.). Soil and Water: Physical Principles and Processes,
1971
V. B. YOUNGER and C. M. McKELL (Eds.). The Biology and Utiliza-
tion of Grasses, 1972
J. B. MUDD and T. T. KOZLOWSKI (Eds.). Responses of Plants to
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R. DAUBENMIRE (Ed.). Plant Geography, 1978
J. LEVITT (Ed.). Responses of Plants to Environmental Stresses, 2nd
Edition.
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Volume II: Water, Radiation, Salt, and Other Stresses, 1980
J. A. LARSEN (Ed.). The Boreal Ecosystem, 1980
S. A. GAUTHREAUX, JR. (Ed.). Animal Migration, Orientation, and
Navigation, 1981
F. J. VERNBERG and W. B. VERNBERG (Eds.). Functional Adapta-
tions of Marine Organisms, 1981
R. D. DURBIN (Ed.). Toxins in Plant Disease, 1981
C. P. LYMAN, J. S. WILLIS, A. MALAN, and L. C. H. WANG (Eds.).
Hibernation and Torpor in Mammals and Birds, 1982
T. T. KOZLOWSKI (Ed.). Flooding and Plant Growth, 1984
E. L. RICE (Ed.). Allelopathy, Second Edition, 1984
M. L. CODY (Ed.). Habitat Selection in Birds, 1985
R. J. HAYNES, K. C. CAMERON, K. M. GOH, and R. R. SHER-
LOCK (Eds.). Mineral Nitrogen in the Plant-Soil System, 1986
T. T. KOZLOWSKI, P. J. KRAMER, and S. G. PALLARDY (Eds.).
The Physiological Ecology of Woody Plants, 1991
H. A. MOONEY, W. E. WINNER, and E. J. PELL (Eds.). Response of
Plants to Multiple Stresses, 1991
List continues at the end of this volume
F l ux
C o n t r ol
in B i o l o g i c al
S y s t e ms
From Enzymes to
Populations
and Ecosystems
Edited by
E.-D. Schulze
Lehrstuhl fur Pflanzenôkologie
Universitàt Bayreuth
Bayreuth, Germany
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Front cover photograph: Casparian bands in the endodermis and exodermis of a maize root
section stained with the fluorescent dye, berberine sulfate, according to the procedure of
Brundrett et al. (1989) (courtesy of C. A. Peterson, University of Waterloo, Ontario,
Canada). For details see Chapter 8, Figure 10B.
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Library of Congress Cataloging-in Publication Data
Flux control in biological systems from enzymes to populations and
ecosystems / edited by E. -D. Schulze.
p. cm. —(Physiological ecology)
Includes bibliographical references and index.
ISBN 0-12-633070-0
1. Biological control systems. 2. Ecophysiology. 3. Plant
physiology. I. Schulze, E. -D. (Ernst-Detlef), Date II. Series.
QH508.F58 1994
581 . l'88--dc20 93-4172
CIP
PRINTED IN THE UNITED STATES OF AMERICA
93 94 95 96 97 98 QW 9 8 7 6 5 4 3 2 1
Contributors
Numbers in parentheses indicate the pages on which the authors' contributions begin.
E. Beck (3, 57, 471), Lehrstuhl fur Pflanzenphysiologie, Universitât
Bayreuth, 95440 bayreuth, Germany
R. Horn (335) Institut fur Pflanzenernâhrung und Bodenkunde, Chris-
tian-Albrechts-Universitàt, 23 Kiel, Germany
U. Jensen (447), Lehrstuhl fur Pflanzenôkologie und Systematik, Uni-
versitât Bayreuth, 95440 Bayreuth, Germany
I. Kôgel-Knabner (303) Lehrstuhl fur Bodenkunde und Bodenokologie,
Fakultat fur Geowissenschaften NA6/134, Ruhr-Universitât Bochum,
463 Bochum, Germany
E. Komor (153), Lehrstuhl fur Pflanzenphysiologie, Universitât Bay-
reuth, 95440 Bayreuth, Germany
C. Schâfer (37), Lehrstuhl fur Pflanzenphysiologie, Universitât Bay-
reuth, 95440 Bayreuth, Germany
R. Scheibe (3), Lehrstuhl Pflanzenphysiologie, Universitât Osnabrùck,
45 Osnabrùck, Germany
E.-D. Schulze (57, 203, 421, 471), Lehrstuhl fur Pflanzenôkologie, Uni-
versitât Bayreuth, 95440 Bayreuth, Germany
E. Steudle (237, 471), Lehrstuhl fur Pflanzenôkologie, Universitât
Bayreuth, 95440 Bayreuth, Germany
M. Stitt (13, 57, 471), Botanisches Institut, Universitât Heidelberg, 69
Heidelberg, Germany
W. Zech (303), Lehrstuhl fur Bodenkunde, Universitât Bayreuth, 95440
Bayreuth, Germany
H. Zwôlfer (365, 421, 447, 471), Lehrstuhl fur Tierôkologie, Universitât
Bayreuth, 95440 Bayreuth, Germany
xiii
Preface
Many factors have influenced our understanding of global biomass pro-
duction. First, the International Biological Program (IBP, 1966-1976)
assessed biomass in ecosystems representative of all the climactic regions
of the globe, and estimated turnover of biomass. Later, when forest
damage by acid rain became apparent, ecologists began to appreciate
that the flux of material was at least as important as pool sizes. The
fluxes of water, nutrients, and carbon explained the long-term effects of
anthropogenic depositions of air pollutants on ecosystems. However, we
were still unable to model these systems because we lacked an understand-
ing of the control of fluxes. At present, this lack of understanding affects
efforts to use modeling in many areas of research, from agriculture to
ecosystem studies. In particular, it restricts us to predicting interactions
of terrestrial ecosystems with the boundary of the atmosphere in terms
of the International Geosphere Biosphere Program.
In 1980, the Deutsche Forschungsgemeinschaft decided to establish a
"Sonderforschungsbereich" (Collaborative Research Center) at the Uni-
versity of Bayreuth. Our aim has been to define general principles of
flux control by comparing patterns and mechanisms of regulation at
various levels of organization, from enzymes to populations and ecosys-
tems. We think that knowledge of such principles will enable us to better
predict human influences on ecosystems. By depicting general patterns
and principles of controls, we hope that we may be able to predict more
quickly and more precisely how ecosystems will respond in a world of
global change.
In this volume, botanists, microbiologists, soil scientists, and zoologists
investigate patterns and mechanisms of matter transfer regulation in
biological systems of different complexity. Based mainly on the experi-
mental results of the long-term research at Bayreuth, this volume contains
significant contributions made by numerous scientists from all parts of
the world. We are very grateful to the Deutsche Forschungsgemeinschaft
for its support of this lengthy research. I should also like to recognize
Steve Halgren for editorial help.
E.-D. SCHULZE
xv
The Malate Valve:
Flux Control at the
Enzymatic Level
R. Scheibe and E. Beck
I. Introduction
The photosynthetic machinery in the thylakoids of autotrophic organisms
converts light energy into the biochemical energy equivalent ATP and
the reducing power equivalent NADPH. Linear electron transport and
photophosphorylation are strictly coupled reactions. The two primary
products of the light reactions, ATP and NADPH, are required to drive
C0 , N0 ~, and S0 2" reduction as well as a great variety of biosynthetic
2 3 4
processes. Despite the large capacity for the generation of ATP and
NADPH, there are two major problems connected with the transfer of
photon flux into biochemical fluxes: (i) The rate of production must fit
the demand and (ii) the turnover of the ATP and NADPH pools must
be controlled separately to compensate for the coupled production and
to attain flexibility with respect to changing requirements by the various
biosynthetic activities in the chloroplast.
II. The ATP to NADPH Balance
Let us consider conditions where there is unlimited photon flux into
the photosynthetic system: A balanced ratio of the ATP and NADPH
production rates should be dictated by the need to achieve an adequate
rate of production of the one metabolite which is in higher demand, and
a concomitant disposal of the excess of the other (see also Stitt, this
volume, Chapter 2). At light-saturated C0 fixation, the limiting compo-
2
Copyright © 1994 by Academic Press, Inc.
FHIX CONTROL IN BIOLOGICAL SYSTEMS 3 All rights of reproduction in any form reserved.
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1. The Malate Valve: Flux Control at the Enzymatic Level 5
nent appears to be ATP. Since ATP production by linear electron flow
is limited by the availability of NADP, cyclic photophosphorylation in
combination with the Mehler reaction (pseudocyclic photophosphoryla-
tion) may support ATP production when the NADPH pool is fully re-
duced (Steiger and Beck, 1981). The hydrogen peroxide formed is finally
detoxified by recycling the electrons from NADPH using the "soluble
electron transport chain" composed of the ascorbate/glutathione redox
system (Groden and Beck, 1979; Halliwell, 1981). However, it seems
likely that this system is only resorted to in the absence of any other
electron acceptor, i.e., in cases of emergency when the system has already
reached a highly reduced ("overreduced") state. This is evident from the
fact that addition of oxaloacetate to isolated chloroplasts as an alternative
acceptor immediately decreases the rate of H 0 production (Steiger and
2 2
Beck, 1981).
The malate valve system, namely the conversion of excess NADPH
into malate by the chloroplast enzyme NADP-malate dehydrogenase can
apparently serve to unload the chloroplast from excess reducing equiva-
lents via export into the cytosol (Heber, 1974). The chloroplast dicarboxy-
late translocator localized in the inner envelope membrane can exchange
malate generated in the stroma for oxaloacetate from the cytosol with
high efficiency (Ebbighausen et aL, 1987). This reaction leads to reoxida-
tion of NADPH inside the chloroplast and export of reducing equivalents
in the form of malate into the cytosol (Fig. 1). Thus, by involving the
cytosol, regulation of the ATP-to-NADPH ratio in the chloroplast can
be achieved (Fig. 2). Further use of the exported reducing equivalents
either in photorespiration (reduction of hydroxy-pyruvate in the peroxi-
1/2 0
2
export
ΐ> from
chloroplast
Figure 2 Poising of the ATP/NADPH ratio by a self-controlled export system for
reducing equivalents ("malate valve").
6 R. Scheibe and E. Beck
somes; Ebbighausen et al, 1987) or in generating energy through uptake
by the mitochondria is then possible. The latter is suggested from the
observation that specific inhibition of the respiratory chain by oligomycin
decreases photosynthetic C0 fixation in isolated protoplasts (Krômer et
2
al, 1988).
The full capacity of the system is rather high: 100 to 200 /xmol of
reducing equivalents per milligram chlorophyll per hour can be con-
verted into transportable malate in C plants. It follows that the potential
3
export of photosynthetic reducing power from the chloroplast via the
malate valve must be strictly controlled, otherwise this export would
deplete stromal NADPH and inhibit the reductive assimilatory steps.
III. Redox Control of the Malate Valve
In the following the components and mechanisms which mediate the
flux through the "malate valve" are described. In contrast to the NAD
(and NADP)-dependent malate dehydrogenases of microorganisms, ani-
mals, and even the extrachloroplastic isoenzymes of plants, the strictly
NADP-dependent plastid enzyme is under redox control. Reduction of
a special regulatory disulfide bridge converts the inactive protein into
the catalytically competent enzyme (Scheibe, 1987). Electrons required
for the reductive activation are sequestered from the photosynthetic elec-
tron transport chain via the ferredoxin/thioredoxin system (Fig. 3) (Bu-
chanan, 1984). As with some other key enzymes of chloroplastic carbohy-
drate metabolism (in addition to the NADP-malate dehydrogenase, the
Calvin-cycle enzymes fructose-1,6-bisphosphatase, sedoheptulose-1,7-
bis-phosphatase, and phosphoribulosekinase and the coupling factor CFj
are converted into catalytically competent forms in the light) the reductive
light modulation acts as an on/off switch (Anderson, 1985). In contrast
to NADP-malate dehydrogenase and the other light-activated enzymes,
the chloroplast glucose-6-phosphate dehydrogenase is converted by pho-
tosynthetic reduction into a form without significant affinity for its sub-
NADP
J v <|
^ V J v f t r^ JVmdh<^ ° 2
Fdox T d
active "
Figure 3 Redox modulation of chloroplast enzymes mediated by the ferredoxin/
thioredoxin system.
1. The Malate Valve: Flux Control at the Enzymatic Level 7
strate glucose-6-phosphate (Scheibe et ai, 1989). Thus functioning of
the oxidative pentose phosphate cycle is prevented at the first step, as
long as photosynthesis is operating (see also Schàfer, this volume, Chap-
ter 3).
IV. A Futile Cycle Provides the Machinery
for Flux Regulation
During photosynthesis, oxygen evolution and the consequent continuous
reoxidation of the light-generated proteinaceous thiols will lead to a futile
cycle of reduction and oxidation of these enzyme forms (see also Komor,
this volume, Chapter 6). The futile cycle, however, creates the basis for
flux control: At a constant rate of reoxidation the portion of reduced
active enzyme is determined by the rate of disulfide reduction by photo-
synthetically energized electrons (Fig. 4). The rate of electron flow to
the target enzyme must be under metabolite control. A comparable prin-
ciple has been described for a protein phosphorylation/dephosphoryla-
tion system (Stadtman and Chock, 1977). A protein kinase phosphorylates
its target enzyme, e. g., mammalian glycogen phosphorylase or glycogen
synthase, while at the same time a protein phosphatase regenerates the
2e,2H+
inactive
H0
2
Figure 4 "Futile cycle" of NADP-MDH (E) which allows adaptation of the enzyme
activity to the actual requirement of the chloroplast for export of reducing equivalents.