Frost Survival of Plants: Responses and Adaptation to Freezing Stress

332 Pages·1987·13.25 MB·English

by  Professor em. Dr. Akira Sakai

A. Sakai . W Larcher
Frost Survival
of Plants
Responses and Adaptation
to Freezing Stress
With 200 Figures
Springer -Verlag
Berlin Heidelberg New York
London Paris Tokyo
Professor em. Dr. AKIRA SAKAI
The Institute of Low Temperature Science
Hokkaido University
Sapporo, Japan
Professor Dr. WALTER LARCHER
Institut flir Botanik der Universitiit Innsbruck
StemwartestraBe 15
A-6020 Innsbruck, Austria
ISBN-13:978-3-642-71747-5 e-ISBN-13:978-3-642-71745-1
001: 10.1007/978-3-642-71745-1
Library of Congress Cataloging in Publication Data. Sakai, A. (Akira), 1920- . Frost survival of
plants. (Ecological studies; v. 62). Bibliography: p. Includes indexes. 1. Plants, Effect of cold on.
2. Plants-Frost resistance. 3. Acclimatization (Plants) 4. Plants-Wounds and injuries. I. Larcher, W.
(Walter), 1929- . II. Title. III. Series. QK156.S235 1981 581.19'165 8fr.31544.
This work is subject to copyright. All rights are reserved, whether the whole or part of the material
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© Springer-Verlag Berlin Heidelberg 1981.
Softcover reprint of the hardcover 1 st edition 1981
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2131/3130-543210
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Preface
Low temperature represents, together with drought and salt stress, one
of the most important environmental constraints limiting the pro
ductivity and the distribution of plants on the Earth. Winter survival, in
particular, is a highly complex phenomenon, with regards to both stress
factors and stress responses. The danger from winter cold is the result
not only of its primary effect, i.e. the formation of ice in plant tissues;
additional threats are presented by the freezing of water in and on the
ground and by the load and duration ofthe snow cover. In recent years,
a number of books and reviews on the subject of chilling and frost
resistance in plants have appeared: all of these publications, however,
concentrate principally on the mechanisms of injury and resistance to
freezing at the cellular or molecular level. We are convinced that analysis
of the ultrastructural and biochemical alterations in the cell and
particularly in the plasma membrane during freezing is the key to
understanding the limits of frost resistance and the mechanisms of cold
acclimation. This is undoubtedly the immediate task facing those of us
engaged in resistance research. It is nevertheless our opinion that, in
addition to understanding the basic physiological events, we should be
careful not to overlook the importance of the comparative aspects of the
freezing processes, the components of stress avoidance and tolerance
and the specific levels of resistance. Frost resistance is a genetically
determined ecophysiological trait which is expressed under environ
mental constraints. The ability to harden is the basis for the differences
between individuals, ecotypes, varieties and species with respect to
their potential frost resistance. The gene pool of every population
exhibits a range of variations both in hardening potential and seasonality
timing, enabling it to survive a certain degree of change in the
environment. The variability of frost resistance within a population is
essential for the survival of a species following frost of unusual severity
or of untimely occurrence, as well as for its adaptation to long-term
fluctuations in climate. The degree of scatter of resistance within the
progeny is characteristic for a species and provides a measure of its scope
and selection. Thus, the quantitative analysis of phenomena over the full
range of their variability among plant groups, species and genotypes
provides important information from the viewpoint of ecology, phylo
genetics and applied science. Climatic stress promotes evolutionary
adaptation and accelerates the differentiation of ecotypes and species.
VI Preface
Progression in the cold hardiness of plants along latitudinal and
altitudinal gradients, and transitions between the various categories of
cold hardiness have been hypothesized as being steps of evolutionary
adaptation to low temperatures during the geological periods in which
colder climates prevailed, as well as being connected with the spread of
plants to colder regions.
The book has been designed to include both the cellular and the
comparative aspects of freezing stress and plant survival. With this
special problem in mind, an attempt has been made to cover the entire
range of ecophysiological research, from the biochemical to an
ecological viewpoint. We have not attempted to produce a comprehen
sive compendium of plant cryobiology, but rather to present data on
responses of plants to freezing stress, drawing to a large extent upon our
personal experience gained in more than three decades of experimental
research. Let us hope that the information presented here will make a
significant contribution to the efforts of investigators engaged in
planning research strategies for the study of plant hardiness in order to
reduce crop losses resulting from frost and related stresses. Furthermore,
it is our hope that more attention than hitherto will be given to the
ecological interpretation of cold stress and cold resistance.
Many colleagues have helped us by means of discussion, by provid
ing us with unpublished data or by placing at our disposal original
photographs and graphs: we gratefully acknowledge the help of
members of the Institute of Low Temperature Science at the Hokkaido
University in Sapporo: S. Yoshida, T. Niki, T. Sato, M. Ishikawa,
M. Uemura, F. Yoshie; of the Hokkaido Forest Tree Breeding Institute:
S. Eiga; and of the Institute of Botany at the University of Innsbruck:
M. Bodner and U. Tappeiner. Further, we should like to express our
thanks to C. J. Weiser and K. Tanino (Oregon State University),
E. L. Proebsting (Washington State University), P. Wardle (DSIR, New
Zealand), A. Kacperska (Warsaw University), M. J. Earnshaw (Univer
sity of Manchester), M. Senser (University of Munich) and E. Beck
(University of Bayreuth) for valuable suggestions and stimulating
discussions. We should also like to take this opportunity to extend our
gratitude to all persons and institutions who have helped us over the
years by sending us their publications. We are most grateful to J. Wagner,
A. Deutsch, R. Gapp and S. Hirn for their assistance in preparing the
manuscript and with the compilation of indices. Our special thanks go
to J. Wieser who has translated part of the text and carefully checked
the remainder.
It is a great pleasure to express our sincere thanks to Dr. K. F.
Springer and the Editor responsible for the Ecological Studies, Prof. Dr.
o. L. Lange, for including our book in their program, also to Dr. D.
Czeschlik and his colleagues at Springer-Verlag for their cooperation
and care in its preparation.
Sapporo and Innsbruck, January 1987 AKIRA SAKAI
WALTER LARCHER
Contents
1. Low Temperature and Frost as Environmental Factors 1
1.1 Low Temperature Hazards. . . . . . . 1
1.2 Cold, Frost, and Snow. . . . . . . . . . 1
1.3 The Occurrence of Cold, Frost, and Snow . 3
1.4 Frost and Snow in the Plant's Environment. 9
1.5 Time of Onset, Severity and Duration of Frost:
The Freezing Risk .. . . . . . . . . . . 15
1.6 Temperature Fluctuations in Wintering Trees . 19
2. The Freezing Process in Plants . . . . . . 21
2.1 Freezing of Water and Aqueous Solutions 21
2.1.1 Ice Nucleation. . . . . . . . . . 21
2.1.2 Freezing of Solutions. . . . . . . 23
2.1.3 Sequence of Events in the Freezing of Liquids 24
2.1.4 Vitrification of Water and Solutes 24
2.2 Freezing of Plant Cells. . . 26
2.2.1 Extracellular Freezing . . 26
2.2.2 Intracellular Freezing. . . 29
2.2.3 Freezing of Intact Tissues. 31
2.2.4 Threshold Freezing Temperature and Supercooling
of Plant Tissues . . . . . . . . . . . . . . . 33
2.2.5 Initiation and Progress of Freezing in the Whole Plant. 36
3. Freezing Injuries in Plants . . . . . 39
3.1 Typology of Freezing Mechanisms 39
3.2 Causes of Death by Freezing . . . 41
3.3 Phenomenology of Frost Damage . 47
3.3.1 Symptoms of Injury . . . . 47
3.3.2 Freezing Damage Peculiar to Trees. 48
3.4 Results of Freezing Injury and Chances of Recovery. 54
4. Mechanisms of Frost Survival. . 59
4.1 Components of Frost Survival 59
4.1.1 Frost Mitigation. . . . 59
VIII Contents
4.1.2 Frost Exclusion . . . . . . . . 62
4.1.3 Components of Frost Resistance. 65
4.2 Supercooling as a Survival Mechanism . 70
4.2.1 Persistent Supercooling of Leaves 70
4.2.2 Deep Supercooling of Xylem Ray Parenchyma Cells 72
4.3 Extraorgan and Extratissue Freezing. . . . . . . 76
4.3.1 Deep Supercooling and Extraorgan Freezing
of Hydrated Seeds . . . . . . . . . . . . 77
4.3.2 Deep Supercooling and Extraorgan Freezing
of Floral Primordia of Woody Angiosperms . 81
4.3.3 Extraorgan Freezing of Conifer Buds. . . . 85
4.4 Comparison and Classification of Frost Survival Mechanisms 89
4.5 Survival at Ultralow Temperatures 91
4.5.1 Desiccated Plant Tissues 91
4.5.2 Hydrated Plant Tissues . . . 93
5. Cold Acclimation in Plants . . . . . . . 97
5.1 The Annual Course of Frost Resistance 97
5.2 The Seasonal Cold Acclimation Process 99
5.2.1 Seasonality Timing. . . . . . . 100
5.2.2 Induction of Cold Acclimation and the First Stage
of the Hardening Process . . . . . . . . . .. 102
5.2.3 The Second Stage of Frost Hardening . . . .. 105
5.3 Environmental Control of the Level of Frost Resistance 107
5.3.1 Fluctuation of Frost Resistance During Winter 108
5.3.2 Water Content of the Plant and Frost Resistance. 112
5.4 Biochemical and Structural Changes During Cold Acclimation 113
5.4.1 Metabolic Pathway Shifts from the Growing State
to the Dormant State. . . . . 113
5.4.2 Sugars and Related Compounds 114
5.4.3 Amino Acids . . . . . . 117
5.4.4 Nucleic Acids and Proteins 118
5.4.5 Lipid Changes. . . . . . 124
5.4.6 Abscisic Acid . . . . . . 132
5.4.7 Cytological Changes During Cold Acclimation. 133
6. Frost Resistance in Plants . . . . . . . . . . . . . .. 138
6.1 Genetic Variation in Frost Resistance . . . . . . . .. 138
6.1.1 Differences in Frost Resistance Between Plant Taxa 138
6.1.2 Differences in Frost Resistance Within Populations. 142
6.1.3 Inheritance of Frost Resistance . . . . . . . .. 153
Contents IX
6.2 Differences in Frost Resistance of Various Plant Organs
and Tissues . . . . . . . 157
6.2.1 Vegetative Organs . . . . . . . . 160
6.2.2 Reproductive Organs. . . . . . . 167
6.3 Ontogenetic Variation in Frost Resistance 168
6.3.1 Variation of Frost Resistance During the Cell Cycle 169
6.3.2 Frost Resistance of Seeds . . . . . . . . . . .. 170
6.3.3 Frost Susceptibility During Germination and at the
Early Seedling Stage . . . . . . . . . . . . .. 171
6.3.4 Frost Resistance During Establishment and Ageing. 172
7. Regional Distribution of Plants and Their Adaptive Responses
to Low Temperatures 174
7.1 Woody Plants Within the Tropics. 175
7.1.1 Mangroves 179
7.1.2 Palms 181
7.2 Evergreen Broad-Leaved Trees and Shrubs 185
7.2.1 Temperate Rain Forest Species 186
7.2.2 Mediterranean Sclerophylls 196
7.3 Transition from an Evergreen to a Deciduous Flora and
Its Consequences for Frost Survival · 200
7.3.1 Woody Plants . .202
7.3.2 Ferns. · 206
7.4 Conifers. · 210
7.4.1 The Freezing Resistance of Various Conifer Families
and Its Connection with Their Distribution Range .211
7.4.2 Characteristics of Freezing Resistance of Conifers .213
7.5 Mountain Plants · 218
7.5.1 Dwarf Shrubs and Herbs of Temperate Mountains · 218
7.5.2 Caulescent Giant Rosette Plants of Tropical High
Mountains .224
7.6 Trends of Adaptive Improvement of Low Temperature
Resistance in Vascular Plants . · 229
8. Winter Damage as the Result of a Complexity of Constraints . 235
8.1 Winter Desiccation . . . . . . . . . . . . . . . . . . 238
8.2 Damage Due to Ice Encasement and Compact Snow .... 251
8.3 Harmful Effects of Heavy and Long-Lasting Snow Cover. . 252
8.4 Winter Survival: A Complex Response. . . . . . . . . . 259
x Contents
Appendix · 260
Determination of Frost Resistance for Comparative Studies · 260
Field Survival . . . . . . . . . · 260
Artificial Freezing Tests . . . . . 261
Analysis of the Freezing Process · 262
Frost Treatment of the Samples · 263
Identification of Frost Injuries . 264
Quantification of Frost Resistance 266
References . . . . . . . . 267
Terminology and Definitions 305
Taxonomic Index 307
Subject Index. . 317