Environmental and Biological Control of Photosynthesis: Proceedings of a conference held at the ‘Limburgs Universitair Centrum’, Diepenbeek, Belgium, 26–30 August 1974

394 Pages·1975·29.96 MB·English

by  O. Björkman (auth.), R. Marcelle (eds.)

Environmental and
Biological Control of Photosynthesis
Environmental and
Biological Control of Photosynthesis
Proceedings of a conference held at the 'Limburgs Universitair
Centrum', Diepenbeek, Belgium, 26-30 August 1974.
Edited by R. Marcelle
Laboratory of Plant Physiology, Research Station of Gorsem,
Sint-Truiden, Belgium.
Dr. W. Junk b.v., Publishers, The Hague, 1975.
Sponsored by:
Het Ministerie van Nationale Opvoeding
Het Nationaal Fonds voor Wetenschappelijk Onderzoek
Het Bestuur van de Provincie Limburg
De Vlaamse Leergangen te Leuven
Het Limburgs Universitair Centrum
Het Opzoekingsstation van Gorsern (LW.O.N.L.)
ISBN-13: 978-90-6193-179-9 e-ISBN-13: 978-94-010-1957-6
DOI: 10.1007/978-94-010-1957-6
© Dr. W. Junk b.v., Publishers, The Hague
Softcover reprint ofthe hardcover 1st edition 1797
Cover design: Max Velthuijs
CONTENTS
Preface ..................................................... VII
O. BJORKMAN, Environmental and Biological Control of Photosynthesis:
Inaugural Address ......................................... .
J.L. PRIOUL, A. REYSS & P. CHARTIER, Relationships between Carbon
Dioxide Transfer Resistances and some physiological and anatomical
Features ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
LJ. LUDWIG, D.A. CHARLES-EDWARDS & A.C. WITHERS, Tomato
Leaf Resistance and Respiration in various Light and Carbon Dioxide
Environments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
D.A. CHARLES-EDWARDS & L.J. LUDWIG, The Basis of Expression of
Leaf Photosynthetic Activities ..... . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37
W.L. OGREN, Control of Photorespiration in Soybean and Maize ........ 45
J.D. HESKETH, J.M. McKINION, J.W. JONES, D.N. BAKER, H.C. LANE,
A.C. THOMPSON & R.F. COLWICK, Problems in building Computer
Models for Photosynthesis and Respiration ....................... 53
K.J. TREHARNE & C,J. NELSON, Effect ofGrowth Temperature on Pho-
tosynthetic and Photorespiratory Activity in TaH Fescue ............ 61
G. HOFSTRA & J.D. HESKETH, The Effects of Temperature and CO2
Enrichment on Photosynthesis in Soybean . . . . . . . . . . . . . . . . . . . . . . . . 71
W.J.S. DOWNTON & J.S. HAWKER, Response of Starch-Synthesis to
Temperature in Chilling-sensitive Plants ......................... 81
J. POSKUTA & A. FRANKIEWICZ-JOZKO, Enhanced Dark CO2 Fixation
by Maize Leaves in Relation to Previous Illumination and Oxygen Con-
centration ................................................ 89
H. GRAHL & A. WILD, Studies on the Content ofP 700 and Cytochromes
in Sinapis alba duringGrowth under two Different Light Intensities .... 107
A. WILD, W. RUHLE & H. GRAHL, The Effect of Light Intensity during
Growth of Sinapis alba on the Electron-Transport and the Noncyclic
Photophqsphorylation ....................................... 115
J.H. TROUGHTON; D.C. FORK & F.H. CHANG, Environmental Effects on
the Membrane associated Electron Transport Reactions of Photosyn-
thesis* ................................................... 387
M.M. LUDLOW, Effect of Water Stress on the Decline of Leaf Net Photo-
synthesis with Age .......................................... 123
M. MOUSSEAU, The Effect of Daylength on daily CO2 Balances of Sinapis
alba L. ................................................... 135
C.L. HEDLEY & D.M. HARVEY, The Involvement of CO2 Uptake in the
Flowering Behaviour of Two Varieties of Antirrhinum majus ......... 149
R. KANDELER, B. HüGEL & TH. ROTTENBURG, Relations between
Photosynthesis and Flowering in Lemnaceae ...................... 161
D.1. DICKMANN, D.H. GJERSTAD & J.C. GORDON, Developmental Pat-
terns of CO2 Exchange, Diffusion Resistance and Protein Synthesis in
Leaves of Populus X euramericana .............................. 171
P.H. HOMANN, Carbon Dioxide Exchange of Young Tobacco Leaves in
Light and Darkness ......................................... 183
P. HOFFMANN & ZS. SCHWARTZ, Characterization of Regulative Inter
actions between the Autotrophie and Heterotrophie System in Phasolus
vulgaris and Triticum aestivum seedlings ......................... 191
J. POSKUTA, E. PARYS, E. OSTROWSKA & E. WOLKOWA, Photosyn
thesis, Photorespiration, Respiration and Growth of Pea Seedlings treated
with Gibberellic Acid (GA3) .•..•............................. 201
G. OBEN & R. MARCELLE, The Effects of CCC and GA on some Bio-
chemical and Photochemical Activities of Primary Leaves of Bean Plants 211
J-M. MICHEL, Effects of CCC on Photosynthesis in Euglena ............ 217
P.E. KRIEDEMANN & B.R. LOVEYS, Hormonal Influences on Stomatal
Physiology and Photosynthesis ................................ 227
N.O. ADEDIPE, Aspects of 14C-Sucrose Translocation ProfIles in Hibuscus
sculentus L (O~(fa) .......................................... 237
J.H. TROUGHTON, Light Level and the Mean Speed of Translocation in
Zea mays Leaves* .......................................... 373
I. ZELITCH, Environmental and Biological Control of Photosynthesis: Ge-
neral Assessment ........................................... 251
Special Session on Crassulacean Acid Metabolism
J.W. BRADBEER, W. COCKBURN & S.L. RANSON, The Labelling of the
Carboxyl Carbon Atoms of Malata in Kalanchoe crenata Leaves ....... 265
W. COCKBURN & A. McAULAY, The Pathway of Malate Synthesis in
Crassu1acean Acid Metabolism ................................. 273
M. KLUGE, L. BLEY & R. SCHMID, Malate Synthesis in Crassulacean Acid
Metabolism (CAM) via a Double CO Dark Fixation? .............. 281
2
S.R. SZAREK & I.P. TING, Photosynthetic Efficiency of CAM Plants in
Relation to C3 and C4 Plants .... . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 289
T.F. NEALES, The Gas Exchange Patterns of CAM Plants ...... . . . . . . .. 299
C.B. OSMOND, Environmental Control of Photosynthetic Options in Cras-
sulacean Plants ...... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 311
J.C. LERMAN, How to Interpret Variations in the Carbon Isotope Ratio of
Plants: Biologie and Environmental Effects ....................... 323
B.G. SUTTON, Control ofGlycolysis in Succulent Plants at Night ....... 337
R. MARCELLE, Effect of Photoperiod on the CO and O Exchanges in
2 2
Leaves of Bryophyllum daigremontianum (Berger) ................. 349
O. QUEIROZ, Rhythmical Characteristics at Different Levels of CAM Regu-
lation: Physiologie al and Adaptive Significance .................... 357
J.W. BRADBEER, A Personal Assessment of the State of Knowledge of
Crassulacean Acid Metabolism (CAM) ........................... 369
Author Index 405
Subject Index 407
* The manuscripts of these two papers were received so late that it was only possible to
inc1ude them at the end of the book in order to avoid a delay in the publication of the
proceedings.
PREFACE
This book reports the proceedings of a meeting held in the 'Limburgs Universitair
Centrum' , Diepenbeek, Belgium, August 26 to 30, 1974. In convening this meet
ing, my aim was to bring together a small number of specialists working on
photosynthesis of course but also always keeping in mind that plants are in
fluenced by their environment (temperature, light quality and intensity, air com
position, daylength ..... ) and can differently react according to their stage of deve
lopment. In general, all these specialists work on whole plants cultivated in well
known conditions (they are not 'market spinach specialists') but, when necessary,
they don't give up the idea of measuring photochemical activities in isolated
chloroplasts, enzyme kinetics ... etc. It is noticeable that about 50% of them are
working in laboratories directly involved with applied research in agriculture or
forestry.
The format of the meeting was intentionally kept small but it allowed generous
time for discussion; thanks are due to Drs. O. BJÖRKMAN, J.W. BRADBEER,
M.M. LUDLOW and C.B. OSMOND for taking the chairs during these discussions.
In such a small meeting, the choice of invited scientists was really a personnal one
and thus reflected my own fields of interest. When planning the conference, I was
continually divided between the wish for inviting other interesting people and the
necessity of keeping time free for discussions.
The meeting would never took place without the active collaboration of the
'Limburgs Universitair Centrum' which not only gave us the hospitality in its new
building but also undertook much of the responsibility for raising funds. This
support and the sponsorships of all organisms listed before are gratefully acknow
ledged. Particular thanks are due to Dr. H. CLUSTERS and Mr. G. OBEN for their
help in the planning and arrangements of the meeting.
R.MARCELLE
Sint-Truiden
March 15, 1975
ENVIRONMENTAL AND BIOLOGICAL CONTROL OF
PHOTOSYNTHESIS:
INAUGURAL ADDRESS
o. BJÖRKMAN
Carnegie Institution of Washington, Stanford, California, 94305 U.S.A.
It is certainly a pleasure, and a privilege to be invited to this meeting on Environ
mental Control of Photosynthesis, a topic that lies very elose to my heart. Regard
less of what our individual motivations for working in this particular field of
research may be I am sure that all of the members of the audience agree that this
is indeed a very important field for many reasons.
As is weIl known, nearly all chemical energy and organic carbon and every bit
of food that enter into any ecosystem on earth is provided by photosynthesis. As
a result, all biological activity from the simplest virus to man is ultimately limited
by how weIl photosynthesis iS' able to operate in all of the very diverse environ
ments that exist on this earth. It is therefore very important to workers in many
branches of biology to know what the environmental restraints and the adaptive
limits of photosynthesis are as weH as to understand what the various mechanisms
that underlie photosynthetic adaptation are and how they work.
Such information is of course also of utmost importance to applied research
concerned with improvement of the productivity and efficiency of agricultural
crops. Increasing population pressures have resulted in a world-wide demand for
an increased production of food. Unfortunately, with currently available crop
plants and modern agricultural practices an increased production would require a
greatly increased input of oil and other limited and costly sources of fossil fuel
energy and would also require that land, now considered marginal or even unsuit
able for cultivation, be utilized. Estimates show that in today's technologically
highly advanced agriculture in the United States the energy content of fossil fuels
(products of past photosynthetic activity) used in the production of food crops
may exceed the energy content of this food. An increase in food production, or
even maintaining it at the present level, will therefore require an increase in the
efficiency of primary productivity in using limited resources. It is a sobering
thought that when our fossil fuel reserves are depleted current photosynthesis may
have to provide not only the food, but also much of the fuel, the elothing and
many essential raw materials. Knowledge of the environmentallimitations and
adaptive mechanisms 01' photosynthesis would provide a basis for the selection
and breeding of plants with improved productivity and improved efficiency in
utilizing water and fertilizers in different elimatic regions. Spending money on
research with the objective of providing information on environmental and bio
logical control of photosynthesis is certainly not extravagant.
During the past 25 years tremendous progress has been made in uncovering the
basic mechanisms of the photosynthetic process. However, whereas in the early
days environmental and adaptive aspects of photosynthesis were in the main
stream of photosynthesis research, in the past-World War II period they have been
treated somewhat like a step-child. Fortunately, I believe this trend has now been
reversed and the fact that we are gathered hefe to exchange results and views in a
conference entirely devoted to Environmental and Biological Control of Photo
synthesis is, indeed, a sure sign that this is so.
One of the main reasons for the relatively slow development of our research
area in the past-World War 11 period was the necessity of specialization in order to
do research on the basic mechanisms of photosynthesis. This led not only to a
compartmentation of research efforts but it also necessitated a strict limitation in
the choice of experimental materials and the bulk of information on the me
chanism of photosynthesis has been obtained from work on spinach chloroplasts
and laboratory strains of green algae, notably Chorella. This limitation of experi
mental materials was probably one of the factors that contributed to the rapid
progress in research on the basic mechanisms of the process at the subcellular
level. However, in part because of this limitation this research did not shed much
light on environment-process interactions, nor did it provide much information on
the extent and mechanisms of genetically based adaptive differentiations that
exist among plants occupying contrasting environments. Unquestionably, this
limited choice of plants was the primary reason why C4 photosynthesis which
characterizes very large and important groups of plants, ineluding many valuable
crops, remained undiscovered for so long.
On the other side of the fence are the whole-plant physiologists, plant breeders
and plant ecologists concerned with environmental aspects of photosynthesis and
productivity. These workers are faced with a multitude of problems requiring the
applications of a wide range of methods for measurements of micrometeorological
factors, energy, water, carbon and nutrient fluxes in the field, and must take
into account a host of interacting environmental variables, and the effects of plant
structure and developmental stage, stomatal behavior and plant water relations, to
mention only a few. It is easy to understand that these workers are often unable,
poorly equipped or at least reluctant to carry their studies to lower levels than the
whole plant or leaf.
It would seem that the ideal solution to this problem would be a elose collabo
ration between the environmentally oriented plant scientists, working at higher
levels of organization, and the mechanism-oriented biochemists and biophysists
working at the cellular and molecular levels. Unfortunately, such collaboration has
been rare, probably mainly because these specialists have come too far apart in
concepts, terminology and knowledge of one anothers fields even to be able to
communicate in a meaningful way. Building bridges between the workers in these
branches of photosynthesis research would probably be very profitable to our
understanding of environmental and adaptive aspects of photosynthesis. As in
bridge construction in general, this bridge building should be undertaken from
both sides of the abyss. As one of those who have tried to put in a brick here and
there I am very glad to see that such a bridge construction is no longer a rare
event. Undoubtedly, the discovery of the C pathway of photosynthesis was an
4
important factor in stimulating a resurgence of interest in studies of environ
mental, evolutionary and adaptive aspects of photosynthesis in general, even
among specialists who are primarily concerned with the basic photochemical and
biochemical mechanisms of the process.
Our knowledge of environmental responses and adaptive differentiation of pho
tosynthesis has been derived largely from studies on econornically important,
2
cultivated plants and until only a few years aga these studies were mosdy restrict
ed to plants of the temperate regions of northern Europe and North America. The
reasons for this are not difficult to understand and need not be enumerated. As
far as short-term objectives are concerned it certainly seems reasonable that
priority is given to research that yields information on those economically import
ant plants which constitute the backbone of the agriculture and forestry of the
countries supporting the research.
However, if the objective is to gain an understanding of the environmental and
evolutionary limits of adaptation of the photosynthetic process and of the physic
al, structural and molecular mechanisms involved, then we should obviously
choose plants which are native to environments which are extreme in one respect
or another as far as photosynthesis is concerned. Such information would provide
a good foundation for the development of new crop plants, particularly for the
world's marginal lands and in evaluating the extent to which the photosynthetic
efficiency of already existing ones can be improved.
The use of wild plants for these studies also has an advantage additional to
providing a greater choice of environmental extremes and therefore a higher
prob ability of discovering adaptive mechanisms. It also avoids a problem that may
exist with cultivated plants, namely that man in his breeding for varieties that
possess certain desirable features may have altered adaptive characteristics that are
important in a stress environment.
When comparing photosynthetic efficiencies of different species or genotypes it
is important to remember that the criteria for efficiency depend on the particular
environment under consideration, and one must also take into account the bio
synthetic cost of producing and maintaining the photosynthetic machinery itself.
Photosynthetic rates, determined under some arbitrary environmental conditions,
or expressed on some arbitrary basis such as leaf area or fresh weight alone, may
be misleading when used as a criterion for comparing photosynthetic efficiencies.
For example, in a densely shaded environment it is the efficiency with which the
plant is able to absorb and utilize light of low intensities which is important. What
the photosynthetic capacity at high light may be or how much water is spent per
amount of CO2 fixed are at most of secondary importance. Also, if two plants
have the same light-harvlsting capacities and quantum yields per unit leaf area,
then it is of course the plant which has invested the least in proteins and other
constituents of the photosynthetic apparatus that is the most efficient one under
these particular conditions (cf. paper by Charles-Edwards, this volume).
The criteria for photosynthetic efficiency in another extreme of habitats such
as hot arid deserts and semi-deserts are obviously quite different. Here radiant
energy is abundant but water supply is limited and the high thermal load together
with a low atmospheric humidity results in a very high water vapor press ure
gradient between the leaves and the surrounding air. The water loss for a given
stomatal conductance to gaseous diffusion thus becomes extremely high. In this
environment it is the ability of the photosynthetic machinery to tolerate and to
operate effectively at high temperatures and high irradiance levels, and the
efficiency with which the plants is capable of fixing CO2 in relation to trans
pirational water loss which are of overriding importance.
I believe that intensive comparative studies on carefully selected, wild plants,
native to extreme natural habitats, is a most powerful and effective approach that
3
we have only begun to make use of. Such studies should ideally include a critical
analysis of the respective environments in terms that are pertinent to photosyn
thesis. They should also include studies of photosynthetic performance in the
field as well as in a range of controlled environments. They should also be
compared with the response of growth. Kinetic analyses of photosynthetic gas
exchange characteristics, although valuable in themselves, become much more
powerful when they are combined with studies of the component reactions of
photosynthesis, the structure of the photosynthetic apparatus and composition of
its constituen ts.
For the remainder of my time this evening I will take the opportunity to
review a few examples that illustrate how strikingly different the photosynthetic
characteristics of plants from contrasting environments can be. I will limit myself
to certain aspects of adaptation to extremes of light and temperature. I will first
discuss the well-known differentiation of sun and shade plants.
Light, the driving force of photosynthesis, shows a very wide variation among
habitats occupied by higher plants. Recent studies in Queensland rain forest have
shown that plants native to the densely shaded forest floor such as Alocasia
macrorrhiza, a C3 plant of the Arum family, are capable of net photosynthesis
and sustained growth in sites where the average daily quantum flux (400-700 nm)
is only 22 tleinstein cm-2day-l, including the contribution of sunflecks (Björkman
& Ludlow, 1972). This compares with a daily flux of about 4500 tleinstein
cm-2day-l in an open habitat on the Califomia coast, which is occupied by a
greater number of species, includingAtriplex hastata (C3, Chenopodiaceae). Even
higher values, about 6600 tleinstein cm-2day-l, have been recorded on the sun
baked desert floor of Death Valley, California, during the summer months when
growth of Tidestromia oblongifolia, a C plant of the Amaranth family, is at the
4
peak (Björkman, unpublished). The quantum flux received by this plant thus
exceeds that received by Alocasia in its rain forest habitat by a factor of about
300.
Figure 1 shows the striking differences that exist in the light dependence of
these three plants when grown under the light intensity regimes of their natural
habitats. The arrows indicate the average maximum light intensities to which the
plants were exposed during growth. In the extreme shade plant dark respiration is
very low and light compensation is reached at extremely low light levels. Although
light saturation occurs at very low light levels it is never reached in this extreme
rainforest habitat. The sun plants, because of their higher respiratory rates would
never even reach light compensation under these conditions. On the other hand
the sun plants have much higher capacity of utilizing high light intensities. In
Tidestromia light saturation is not reached even in full noon sunlight and the light
saturated rate is about 15 tim es higher than in Alocasia. While it is not difficult to
see that high capacity for photosynthesis is advantageous in high light intensity
environments it does not direct1y follow that it would be disadvantageous in low
intensity environments. However, as I will show in amoment, a high capacity of
light-saturated photosynthesis requires a greater investment in several leaf
constituents including photosynthetic enzymes and electron carriers and this cost
would obviously be disadvantageous since there would be no return on this greater
investment. Moreover, maintenance of this high-capacity machinery presumably
requires an increased rate of oxidative phosphorylation and hence an increased
4