Crassulacean Acid Metabolism: Biochemistry, Ecophysiology and Evolution

473 Pages·1996·28.35 MB·English

by  K. Winter

Ecological Studies, Vol. 114
Analysis and Synthesis
Edited by
O.L. Lange, Wiirzburg, Germany
H.A. Mooney, Stanford, USA
Ecological Studies
Volumes published since 1989 are listed at the end of this book.
Springer
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K. Winter 1.A.C. Smith (Eds.)
Crassulacean Acid
Metabolism
Biochemistry, Ecophysiology
and Evolution
With 123 Figures and 45 Tables
Springer
Dr. Klaus Winter
Smithsonian Tropical Research Institute
P.O. Box 2072, Balboa
Republic of Panama
Dr. J. Andrew C. Smith
Department of Plant Sciences
University of Oxford
South Parks Road
Oxford OXl 3RB,
and Magdalen College
Oxford OXl 4AU
UK
Front cover: The cover motif shows CAM plants in southern Madagascar, with a
simplified scheme of the CAM cycle superimposed. The "spiny forest" of Madagas
car represents a high-biomass community of CAM plants, comprised principally of
succulent members of the Didiereaceae up to 10m tall (Alluaudia ascendens,
A. dumosa, A. procera) and Euphorbiaceae (Euphorbia leucodendron, E. oncoclada,
E. plagiantha, E. stenoclada) with species of Crassulaceae (Kalanchoe spp.), Aspho
delaceae (Aloe spp.) and Cucurbitaceae (Xerosicyos danguyi) in the undergrowth.
ISBN-13: 978-3-642-79062-1 e-ISBN-13: 978-3-642-79060-7
DOl: 10.l0071 978-3-642-79060-7
Library of Congress Cataloging-in-Publication Data. Crassulacean acid metabolism: biochemistry,
ecophysiology, and evolution/Klaus Winter, J. Andrew C. Smith (eds.). p. cm. - (Ecological stu
dies: vol. 114) Papers from an International Workshop on Crassulacean Acid Metabolism, held at
Smithsonian Tropical Research Institute, Republic of Panama, Mar. 21-26, 1993. Includes biblio
graphical references and index. ISBN 978-3-642-79062-1. Crassulacean acid metabolism-Congresses. I.
Winter, Klaus, 1949- . II. Smith, J.A.c. (J. Andrew C.). III International Workshop on Cras
sulacean Acid Metabolism (1993: Smithsonian Tropical Research Institute, Republic of Panama) IV.
Series: Ecological studies: V. 114. OK881.C73 1996 581.5-dc20 95-7373
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Dedicated to the memory of
Alan P. Smith
(1945-1993),
a pioneer in plant ecophysiology.
Preface
Crassulacean acid metabolism (CAM) is one of the classic examples of
a metabolic adaptation to environmental stress. Well over 5% of vas
cular plant species engage in this water-conserving photosynthetic
pathway to obtain carbon for growth and reproduction. Intensified
research activity over the last few years has led to major advances in
understanding the biology of CAM plants - from their biochemistry
and molecular biology to fundamental aspects of their physiology,
ecology and evolution. While a holistic approach characterized CAM
research in the past, recent studies have become ever more specialized
and analytical. CAM research is ready for a detailed review that
attempts to integrate these new developments.
This book has its origins in an International Workshop on Cras
sulacean Acid Metabolism held at the Tupper Conference Center of
the Smithsonian Tropical Research Institute (STRI), Republic of Pa
nama, from March 21 to 26, 1993. Over 60 scientists came together to
review and discuss recent developments in their research. More than a
decade had elapsed since the last major meeting on CAM plants, held
at the University of California at Riverside in January 1982. Since
then, important new areas of research have emerged. These include
studies of gene expression and the molecular basis of CAM, of the
ecophysiology of tropical epiphytes and other CAM plants in their
natural environments, of the productivity of several agronomically
important species, and of CAM in submerged aquatic species. Today,
it is no longer possible to regard CAM as "a rather eccentric phenom
enon displayed by a small group of xeromorphic plants", as an emi
nent plant physiologist wrote as recently as 1987. We hope this book
will provide a coherent overview of the rapid advances that have been
made in this field and of our current understanding of CAM.
We are indebted to the Smithsonian Tropical Research Institute for
making funds available for organizing the workshop in Panama, and
especially to the Director, Ira Rubinoff, for his continual support and
encouragement. Many members of the STRI staff, in particular
Monica Alvarado, Maria Luz Calderon and Gloria Maggiori, deserve
special thanks for an enormous amount of assistance throughout the
meeting. We all owe a great debt to our late colleague, Alan P. Smith,
VIII Preface
who did so much to establish plant ecophysiology as a research disci
pline at STRI. Alan was heavily involved in the planning of this
workshop, but sadly was not able to participate in the meeting itself.
He was an inspiration to many people at STRI and in the world of
tropical ecophysiology.
The book begins with a summary of the basic principles of CAM to
lay the foundations for three major sections that cover the different
areas of current research. Part A deals with the biochemistry of the
CAM cycle, Part B focuses on the environmental and developmental
control of CAM and underlying molecular mechanisms, while Part C
is devoted to the ecological diversity and evolutionary origins of
CAM. The three sections are followed by a chapter that attempts to
draw together some of these latest findings and to identify research
directions that may be of particular importance in the years ahead.
Because of the large number of CAM plants now known, we have also
compiled a complete list of genera in which CAM has been
documented, with which the book concludes. Overall, we hope the
result is a volume that will be useful both to research scientists and to
advanced students in plant biochemistry, physiology and ecology who
wish to learn more about the metabolic basis of plant adaptation to
environmental stress.
Panama City and Oxford, 1995 Klaus Winter
J. Andrew C. Smith
Contents
An Introduction to Crassulacean Acid Metabolism.
Biochemical Principles and Ecological Diversity
K. Winter and l.A.C. Smith ... 1
Discovery of Dark CO2 Fixation 1
Biochemistry .................... 2
Phenotypic Plasticity ............... 3
Ecophysiology and Species Diversity ...... 6
Conclusions .................... 9
References ....................... 10
Part A: Biochemistry of Carbon Flow
During Crassulacean Acid Metabolism
Preface ................. . 17
1 Stoichiometric Nightmares:
Studies of Photosynthetic O and CO Exchanges
2 2
in CAM Plants
c.B. Osmond, M. Popp, and S.A. Robinson 19
1.1 Introduction ........ . 19
1.2 Simultaneous Measurements
of O2 and C02Exchange
Using an 02/C02 Electrode System 20
1.3 Photosynthetic 02/C02 Stoichiometry
During C Photosynthesis in Phase IV 20
3
1.4 Photosynthetic 02/C02 Exchanges
During Deacidification in Phase III 22
1.5 Photosynthetic 02/C02 Exchanges
During Acidification in Phase I 25
1.6 Conclusions 28
References ............ . 28
x Contents
2 Alternative Carbohydrate Reserves
Usedin the Daily Cycle
of Crassulacean Acid Metabolism
C.C Black, l.-Q. Chen, R.L. Doong,
M.N. Angelov, and S.l.S. Sung 31
2.1 Introduction ........ . 31
2.2 The Division of CAM Plants
into Two Metabolic Groups .......... . 32
2.3 The Use of Soluble Sugars Versus Polysaccharides
as a Carbohydrate Reserve ........ . 32
2.4 Sequences of Biochemical Reactions
in the Daily Use of Hexoses Versus Starch
in CAM ................... . 37
2.5 Bioenergetics in Different Groups of CAM Plants 42
2.6 Conclusions 43
References ....................... . 43
3 Roles of Circadian Rhythms, Light
and Temperature in the Regulation
of Phosphoenolpyruvate Carboxylase
in Crassulacean Acid Metabolism
P.l. Carter, C.A. Fewson, G.A. Nimmo,
H.G. Nimmo, and M.B. Wilkins ... 46
3.1 Introduction .................. 46
3.2 Phosphorylation of PEPC in Intact Tissue 47
3.3 Properties and Regulation
of PEPC Kinase and Phosphatase 48
3.4 Effects of Light and Temperature
on PEPC-Kinase Activity 50
3.5 Conclusions 51
References .......... 52
4 Transport Across the Vacuolar Membrane
in CAM Plants
l.A.C. Smith, 1. Ingram, M.S. Tsiantis,
B.l. Barkla, D.M. Bartholomew, M. Bettey,
O. Pantoja, and A.l. Pennington .... . 53
4.1 Introduction ................... . 53
4.2 Osmotic and Ionic Relations of the Vacuole 54
4.2.1 Osmotic Characteristics ............. . 54
Contents XI
4.2.2 Ionic Characteristics ............ . 54
4.3 Malic Acid Accumulation in the Vacuole 58
4.3.1 Primary Active H + Transport ... 59
4.3.2 Malate Transport into the Vacuole 62
4.3.3 Sodium Chloride Accumulation .. 65
4.4 Malic Acid Remobilization from the Vacuole 65
References .................... . 67
5 The Tonoplast as a Target of Temperature Effects
in Crassulacean Acid Metabolism
M. Kluge and M. Schomburg 72
5.1 Introduction .................... . 72
5.2 Possible Implications
of the Temperature-Dependent Phase Behaviour
of Tonoplast Lipids for CAM .......... . 72
5.3 Experimental Approaches ............ . 74
5.4 Outlook ............... . 75
References ...................... . 76
6 Regulation of Crassulacean Acid Metabolism
in Kalanchoe pinnata as Studied by Gas Exchange
and Measurements of Chlorophyll Fluorescence
U. Heber, S. Neimanis, and W.M. Kaiser 78
6.1 Introduction ................... . 78
6.2 Control of Photosystem II
and of Linear Electron Transport ...... . 79
6.3 Malate Decarboxylation ............. . 84
6.4 Photorespiration ............. . 86
6.5 pH-Sensitivity of Photosynthesis .... . 88
6.6 Proton Transport Across the Tonoplast 90
6.7 Light-Dependent Cytosolic Alkalinization 91
6.8 Metabolic Regulation of CAM 91
6.9 Conclusions 94
References ............ . 95
7 Energy Dissipation and the Xanthophyll Cycle
in CAM Plants
W.W. Adams III and B. Demmig-Adams .. 97
7.1 Introduction ................... . 97
7.2 Energy Dissipation and the Xanthophyll Cycle 98