Crassulacean Acid Metabolism: Analysis of an Ecological Adaptation

219 Pages·1978·8.52 MB·English

by  Professor Dr. M. Kluge

Ecological Studies
Analysis and Synthesis
Edited by
W. D. Billings, Durham (USA) F. Golley, Athens (USA)
O. L. Lange, Wtirzburg (FRG) J. S. Olson, Oak Ridge (USA)
Volume 30
Manfred Kluge · Irwin P. Ting
Crassulacean
Acid Metabolism
Analysis of an Ecological Adaptation
With 112 Figures
Springer-Verlag Berlin Heidelberg New York 1978
Professor Dr. M. KLUGE
Institut fUr Botanik, Technische Hochschule
SchnittspahnstraBe 3-5, 6100 Darmstadt/FRG
Professor I. P. TING
Department of Biology, University of California
Riverside, CA 92521/USA
ISBN-13: 978-3-642-67040-4 e-ISBN-13: 978-3-642-67038-1
DOl: 10.1007/978-3-642-67038-1
Library of Congress Cataloging in Publication Data. Kluge, Manfred, 1936-. Crassulacean acid metabolism.
(Ecological studies; v. 30). Bibliography: p. Includes index. 1. Crassulacean acid metabolism. 2. Acclimatization
(Plants). 3. Botany-Ecology. 1. Ting, Irwin P.,joint author. II. Title. III. Series. QK881.K56.582'OI'33.78-12658.
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© by Springer-Verlag Berlin· Heidelberg 1978
Softcover reprint of the hardcover 1st edition 1978
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Acknowledgments
The preparation of this monograph would not have been possible without our
many colleagues, associates, and students who contributed so much to our
understanding of the physiology and ecology of Crassulacean Acid Metabolism
plants. We are most grateful to Ph. Chimiklis, Z.Hanscom, O. L. Lange, U. Llittge,
R. Marcelle, S. K. Mukerji, T. Neales, C. B. Osmond, O. Queiroz, B. Sutton, and
S. Szarek who contributed directly. Our colleagues P. N. Avadhani, W. Laetsch,
W. W. Thomson, D.J. v. Willert, and K. Winter were generous in allowing us to use
unpublished photographs and micrographs. We also thank Rosalia Heger, Doris
Schafer, and Fanita Terry for preparation of many figures throughout the text.
Further, we must express our appreciation to the Deutsche Forschungsgemein
schaft and the U. S. National Science Foundation for financial support of our
own personal research programs on CAM. The Botanic Gardens at the Uni
versity of California, Berkeley, has been most generous in allowing the use of
facilities and access to succulent plants. Our manuscript, of course, was not
complete until typed by Inge Hill and Irene Schmidt, to whom we are grateful.
Finally, we must thank Konrad Springer for his help and encouragement during
the preparation of the manuscript.
December, 1978 MANFRED KLUGE
IRWIN P. TING
Contents
Introduction. 1
Terminology 3
1. Taxonomy and Geographical Distribution of CAM Plants 5
1.1 Cactaceae. . . 5
1.2 Crassulaceae. . 10
1.3 Euphorbiaceae. 12
1.4 Aizoaceae (Mesembryanthemaceae) . 12
1.5 Bromeliaceae . 15
1.6 Asclepiadaceae . 17
1.7 Orchidaceae. 17
1.8 Liliaceae . 19
1.9 Agavaceae. 21
1.10 Asteraceae 23
1.11 Vitaceae 23
1.12 Geraniaceae . 24
1.13 Other Families. 24
1.14 Conclusions. . 28
2. Morphology, Anatomy, and Ultrastructure of CAM Plants . 29
2.1 What is a Succulent? . . . . . . . . 29
2.2 Quantitative Indices of Succulence. . . 30
2.3 Succulence and the Occurrence of CAM 31
2.3.1 Succulent CAM Plants . . . . . 31
2.3.2 Nonsucculent CAM Plants . . . 34
2.3.3 Mesophyll Succulence (Sm) as a New Index of CAM Capacity? 34
2.4 The Presence of the Photosynthetic Apparatus as a Prior Condition
for the Occurrence of CAM. . . . . . . . . . . . . . . . 37
2.5 The Architecture and Ultrastructure of CAM -Performing Cells 38
2.5.1 Light Microscope Observations 38
2.5.2 Electron Microscope Observations . . . . . . . . . . 38
VIII Contents
3. The Metabolic Pathway of CAM . . 45
3.1 The Processes of the Dark Period 45
3.1.1 Early History . . . . . . 45
3.1.2 Dark CO Fixation and Its First Product 46
2
3.1.3 Secondary Products and Organic Acids Other Than Malic 48
3.1.4 The Active Chemical Species of "C02" . • • . • . • . 50
3.1.5 Generation of P-Enolpyruvate, the CO Acceptor in Dark
2
CO Fixation . . . . . . . . 52
2
3.1.6 Depletion of Malate in the Dark 55
3.1.7 The Storage of Malic Acid. . . 55
3.2 The Processes of the Light Period . . 56
3.2.1 Deacidification and Malate Decarboxylation. 56
3.2.2 The Fate of the Decarboxylation Products . 58
3.2.2.1 Three-Carbon Fragments. . . . . 58
3.2.2.2 Carbon Dioxide. . . . . . . . . 58
3.2.3 Assimilation of Exogenous CO in the Light 60
2
3.2.4 Photorespiration in CAM Plants . . 61
3.3 Carbon Isotope Composition . . . . . . . . . 63
3.4 The Proposed Total Carbon Flow in CAM . . . 65
3.5 Comparison of CAM with Other Carboxylation Pathways in Plants 67
3.5.1 The Nonautotrophic C Pathway of CO Fixation 67
4 2
3.5.2 C -Photosynthesis 68
3
3.5.3 C -Photosynthesis . . . . . . . . . 69
4
3.5.4 Conclusions. . . . . . . . . . . . 71
3.6 Translocation of CAM Products in the Plant 71
4. Control and Modification of CAM 73
4.1 Definitions. . . . . . . . 73
4.2 Metabolic Control of CAM. 73
4.2.1 The CAM Enzymes. . 73
4.2.1.1 P-Enolpyruvate Carboxylase [Orthophosphate: Oxal
acetate Carboxylase (Phosphorylating)]. . . . . . . 73
4.2.1.2 Malate Dehydrogenase (L-malate: NAD Oxidoreduc-
tase). . . . . . . . . . . . . . . . . . . . 79
4.2.1.3 Aspartate Aminotransferase (L-aspartate: oc-Oxo-
glutarate Aminotransferase) . . . . . . . . . . 80
4.2.1.4 "Malate Enzyme" [L-malate: NADP Oxidoreductase
(Decarboxylating)] . . . . . . . . . . . . . 81
4.2.1.5 P-enolpyruvate Carboxykinase [ATP: Oxalacetate
Carboxylase (Transphosphorylating)] . . . . . 81
4.2.1.6 Pyruvate, Phosphate Dikinase. . . . . . . . . 82
4.2.1.7 Alanine Aminotransferase (L-Alanine: oc-Oxoglutarate
Aminotransferase). . . . . . . . . . . . . ., 82
4.2.1.8 Riboluse-1.5-Bisphosphate Carboxylase/Oxygenase
[3-phospho-D-glycerate Carboxylase (Dimerizing)] . 82
Contents IX
4.2.1.9 Phosphofructokinase (ATP-D-fructose-6-
phosphate-l-phosphotransferase) . . . . 83
4.2.1.10 Phosphorlyase (ex-1.4-Glucan: Orthophosphate
Glucosyltransferase) . . . . . . . . . . . 83
4.2.2 The Compartmentation of CAM Enzymes and Metabolites. 83
4.2.2.1 Enzymes. . 83
4.2.2.2 Metabolites. . . . . . . . 86
4.2.2.3 Conclusions . . . . . . . 87
4.2.3 Models of Metabolic CAM Control. 87
4.2.3.1 Control of CAM During the Dark Period. 87
4.2.3.2 Control of CAM During the Dark/Light Transient and
During the Light Period . . . . . . . . . . . . . 89
4.3 Modification of the Diurnal Malic Acid Cycle by External Factors 94
4.3.1 Effects of Temperature 94
4.3.2 Effects of Light . . . . . . . . . . . . . . . . . . . . 94
4.3.3 Effects of Ions. . . . . . . . . . . . . . . . . . . . . 95
4.3.4 Effects of Water Relations and the Question of "Facultative"
CAM Plants. . . . . . . . . . . . . . . . . . . . . . 97
4.3.4.1 Effects of Drought on CAM in "Obligate" CAM Plants 98
4.3.4.2 Induction of CAM in "Facultative" CAM Plants. 98
4.3.5 Effects of Oxygen and Carbon Dioxide 100
4.3.5.1 Oxygen . . . . 100
4.3.5.2 Carbon Dioxide. . 101
4.4 Seasonal Control of CAM 102
4.4.1 Photoperiod. . 102
4.4.2 Thermoperiod. . . 104
4.4.3 Hydroperiod . . . 105
4.5 Developmental Control of CAM 106
4.6 Conclusions . . . . . . . . . 106
5. Gas Exchange of CAM Plants . 108
5.1 CO Exchange . . . . . 108
2
5.1.1 History. . . . . . 108
5.1.2 General Phenomena of CO Exchange. 109
2
5.1.3 Patterns of CO Exchange in the Dark 111
2
5.1.3.1 General Characteristics. . . . 111
5.1.3.2 Factors Affecting CO Exchange During the Dark
2
Period. . . . . . . . . . . 112
5.1.4 CO Exchange During the Light Period . . . . . . . . .. 120
2
5.1.4.1 General Characteristics. . . . . . . . . . . . . . 120
5.1.4.2 Factors Affecting CO Exchange During the Light
2
Period. . . . . . . . . . . . . . . . . . 120
5.1.4.3 The Initial Burst of CO Uptake. . . . . . . 125
2
5.1.4.4 Compensation Point, Effects of CO and O Concentra-
2 2
tion on CO Fixation in the Light . . . . . . . . . 126
2
x
Contents
5.1.5 CO Exchange in Continuous Darkness or Continuous Light 128
2
5.1.5.1 Introduction . . . . . . . . . . . . . . . 128
5.1.5.2 CO Exchange in Continuous Darkness. . . . 128
2
5.1.5.3 CO Exchange Under Continuous Illumination 131
2
5.1.5.4 Conclusions 132
5.2 Oxygen Exchange. . . . . 134
5.2.1 History. . . . . . . 134
5.2.2 Manometric Analysis. 134
5.2.3 Polarographic Analysis 134
5.2.4 Paramagnetic Analysis 134
5.3 Water Vapor Exchange and Stomata of CAM Plants. 135
5.3.1 Introduction. . . . . . . . . . . . . . 135
5.3.2 The Diurnal Cycle of Stomata Movements. . . 136
5.3.2.1 Phenomenology. . . . . . . . . . . 136
5.3.2.2 Coupling Between CAM and Movements of Stomata. 137
5.3.2.3 Mechanism of Stomatal Opening . 139
5.3.3 Gas Diffusion Resistances in CAM Plants. 140
5.3.3.1 Gas Exchange Parameters . . 140
5.3.3.2 Boundary Layer Resistance (ra) 141
5.3.3.3 Stomatal Resistance (rs) . . . 141
5.3.3.4 Cuticular Resistance (rc) . . . 142
5.3.4 Response of Stomatal Movements to the Age of the Plant and
Environmental Factors . 143
5.3.4.1 Age . . . . . . 143
5.3.4.2 Water Relations. 145
5.3.4.3 Temperature . . 146
5.3.4.4 Light . . . . . 147
5.3.5 Morphology of Stomata in CAM Plants. 148
5.3.5.1 Number and Distribution of Stomata. 148
5.3.5.2 Size and Shape of the Stomata. . . . 148
5.3.6 Thermal Consequences of Stomatal Behavior in CAM Plants. 151
6. Ecology, Productivity, and Economic Use of CAM Plants 153
6.1 The Hypothesis: Ecological Advantage of CAM . 153
6.2 Verification of the Hypothesis. . . 156
6.2.1 CAM and Water Use. . . . . . . . . . 156
6.2.2 Observation of CAM in Situ. . . . . . . 160
6.2.2:1 Gas Exchange and Acid Fluctuation 161
6.2.2.2 Estimations of ,,13 C Values in Samples Collected in the
Field . . . . . . . . . . . . . . . 169
6.2.2.3 Ecological Relevance of Optional CAM. 171
6.2.3 Conclusions. . . 172
6.3 Productivity . . . . . 173
6.4 Economic Exploitation. 177
Contents XI
References 179
Appendix. 199
Taxonomic Index 203
Subject Index 207
List of Abbreviations and Symbols
ABA = abscissic acid NAD+,
Ala = alanine NADH2 = nicotinamide adenine
AMP,ADP, dinucleotide (oxidized,
ATP = adenosine mono-, di-, reduced)
triphosphate NADP+,
Asp = aspartate NADPH2 = nicotinamide adenine
dinucleotide phosphate
CAM = Crassulacean Acid
(oxidized, reduced)
Metabolism
NADP-
b13C = 12Cj13C ratio, index of
TPDH = triosephosphate dehydro-
carbon isotope composi-
genase (N AD P
tion in plant material
dependent)
DAAP = dihydroxyacetone
OAA = oxalacetate
phosphate
o:-OG = o:-oxoglutarate
dm = decimeter Pi = inorganic phosphate
1,3 DPGA= 1,3 diphosphoglyceric PPi = pyrophosphate
acid P = water potential
dwt = dry weight PEP = phosphoenol pyruvate
PEP-C = phosphoenolpyruvate
F-6-P = fructose-6-phosphate
carboxylase
FDP = fructose-l,6-diphosphate
2-PGA = 2-phosphoglyceric acid
fwt = fresh weight
3-PGA = 3-phosphoglyceric acid
GAP = glyceraldehyde-3-
PFK = phosphofructokinase
phosphate
Pyr = pyruvate
o:-D-glu. = o:-D-glucose r = resistance to gas transfer
glu = glutamate RudP = ribulose-l,5-diphosphate
G-I-P = glucose-I-phosphate RQ = respiratory quotient
G-6-P = glucose-6-phosphate S = index of succulence
Sm = index of mesophyll
IRGA = infrared gas analyzer
succulence
J = joule
SWC = soil water capacity
Km = Michaelis con stante TR = transpiration ratio
Mal = malate Vrnax = maximum velocity of
MDH = malate dehydrogenase enzymatically catalyzed
n = index of cooperativity in reactions
the Hill equation VDP = vapor pressure deficit