Lectures on Photomorphogenesis

248 Pages·1972·8.795 MB·English

by  Professor Hans Mohr (auth.)

H. Mohr
Lectures on
Photomorphogenesis
With 219 Figures
Springer-Verlag
Berlin· Heidelberg . New Yark 1972
Professor HANS MOHR
Biologisches Institut II der Universitat
Freiburg i. Br./BRD
For the cover Figs. 2 and 22 of this volume have been used.
ISBN-13: 978-3-540-05879-3 e-ISBN-13: 978-3-642-65418-3
DOl: 10.1007/978-3-642-65418-3
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© by Springer-Verlag Berlin· Heidelberg 1972. Library of Congress Catalog Card Number 72-83443.
Preface
The discovery of the reversible red far-red control of plant growth and development and
the subsequent in vivo identification and isolation of the photoreceptor pigment, phyto
chrome, constitutes one of the great achievements in modern biology.
It was primarily a group of investigators at the Plant Industry Station, Beltsville, Mary
land, headed by the botanist H.A. BORTHWICK and the physical chemist S.B. HENDRICKS,
who made the basic discoveries and developed a theoretical framework on which the current
progress in the field of phytochrome is still largely based.
While the earlier development of the phytochrome concept has been covered by a num
ber of excellent articles by the original investigators [104,105,33,238] as well as by others
who joined the field of phytochrome research later [72, 109, 219], a comprehensive and
up-to-date treatment of photomorphogenesis is not available at present. Since it seems
to be needed for teaching as well as for researchers I have tried to summarize the present
state of the field, reviewing the historical aspects of the phytochrome story only insofar
as they are required to understand the present situation. The emphasis of my treatment
will be on developmental physiology ("photomorphogenesis") rather than on phytochrome
per se.
The opportunity of writing this review was made possible by a Visiting Professorship
granted to me by the University of Massachusetts during the fall term of 1971. The present
text is based on a series of 24 lectures which I delivered at U Mass. I am grateful to my
colleagues in the Department of Botany at U Mass for their cordial reception and continuous
encouragement as well as for the excellent intellectual climate I enjoyed at Amherst.
This book is dedicated to Dr. H.A. BORTHWICK and to Dr. S.B. HENDRICKS. I began
to work with the mustard seedling 15 years ago as a foreign postdoctoral fellow at Beltsville.
The mode of cooperation among the Beltsville group opened my eyes to the benefits of
team-work, and the wisdom, humility and helpfulness of the two senior scientists was
an unforgettable experience which has been a constant inspiration ever since.
Freiburg i. Br. July 1972 H. MOHR
Contents
pt Lecture: Phenomenology of Photomorphogenesis; the Goals of Photomor
phogenic Research; the Operational Criteria for the Involvement of
Phytochrome .......... .
Selected Further Reading . . . . . 12
2nd Lecture: Some Properties of Phytochrome. 13
Selected Further Reading . . . . . 23
3'<1 Lecture: Intracellular Localization of Phytochrome. 24
Selected Further Reading . . . . . . . . . . 36
4th Lecture: Induction Experiments Versus Steady State Experiments; the Problem
of the "High Irradiance Response" (HIR) . 37
1. Some Phenomena . . . . . . . . . . . . . . . . . . . . . . . . . . . 37
2. Some Conclusions .......................... . 40
3. Control of Hypocotyl Lengthening in Lettuce (Lactuca sativa L.,
cv. Grand Rapids) as a Prototype of a "High Irradiance Response" 41
4. Further Applications of HARTMANN'S Technique ......... . 45
5. The Action of Blue Light in "Long-term" Experiments ..... . 45
6. Sequential Action of "High Irradiance Reaction" and Pfr (in the
Ground State)? ........................... . 46
7. HIR and Photosynthesis ...................... . 46
8. Operational Definitions (Criteria) for the Involvement of Phyto-
chrome in a Response. . . . . . . . . . . . . . . . ........ . 47
Selected Further Reading . . . . . . . . . . . . . . . . . . . . . . . . 47
5th Lecture: Phytochrome and the Diversity of Photoresponses; "Positive" and
"Negative" Photoresponses; a Unifying Hypothesis . 48
Selected Further Reading . . . . . . . . . . 59
6th Lecture: Phytochrome-mediated Enzyme Induction ..... . 60
Suggested Further Reading . . . . . . . . . . . .. . 68
7th Lecture: Enzyme Repression, Mediated by Phytochrome through a Threshold
Mechanism ............................... . 69
Selected Further Reading . . . . . . . . . . . . . . . . . . . . . . . . 76
8th Lecture: Phytochrome-mediated Modula'tion of Metabolic Steady States and of
Photonastic Movements . . 77
1. Ascorbic Acid Synthesis . . . . . . 77
2. Carotenoid Synthesis ....... . 79
3. The Problem of the "Lag-phases" . 81
4. Modulations of Specialized Cells .. 83
Selected Further Reading . . . . . . . 87
9th Lecture: Control of Longitudinal Growth by Phytochrome. 88
1. General Remarks . . . . . . . . . . . . . . . . . . 88
VI Contents
2. Interaction or no Interaction between Phytochrome and Gibberel
lic Acid (GA3) in Control of Hypocotyl Elongation in Mustard
Seedlings ............................... 88
3. Is RNA and Protein Synthesis Related to Phytochrome-mediated
Control of Longitudinal Ceil GrO\vth? . . . . . . . . . . . . . .. 90
4. Is Carbohydrate Metabolism Related to Control of Longitudinal
Ceil Growth? . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 95
5. Control by Far-red Light of Hypocotyl Lengthening in Diploid
Tetraploid Seedlings . . 96
6. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 97
Selected Further Reading . . . . . . . . . . . . . . . . . . . . . . .. 97
10th Lecture: Modulation of Hypocotyl Longitudinal Growth by Plr(ground state)
through a Threshold Mechanism. . . . . . . . . . . . . . . . . . .. 98
1. Experimental Data . . . . 98
2. Theoretical Treatment . . 101
3. Growth-limiting Proteins 103
4. A Final Comment. . . . . 103
Appendix: On the Use of Excised Segments in Phytochrome Research 104
Selected Further Reading . . . . . . . . . . . . . . . . . . 104
11 th Lecture: The Problem of the Primary Reaction of Phytochrome. . 105
1. Different Plr Populations. . . . . . . . . . . . . . . . 106
2. Polarotropism of Fern Sporelings . . . . . . . . . . . . 106
3. Threshold Regulation of Lipoxygenase Synthesis vs. Phyto
chrome-mediated Anthocyanin Synthesis as a Graded Response.. 107
4. Control by Pfr (ground statc) of Extension Growth and Antho
cyanin Synthesis in One and the Same Ceil. . . . . . . . . . . .. 107
5. Control by Plr of Ascorbic Acid and Anthocyanin Accumulation
in the Mustard Seedling. . . . . . . . . . . . . . . . . . . . . . .. 108
6. Control of PAL (Phenylalanine Ammonia-lyase) and AO (Ascor-
bate Oxidase) Synthesis in the Mustard Seedling. 110
7. General Conclusions . . . . . . . . 111
8. Tentative Models . . . . . . . . . . 111
9. The Significance of Acetylcholine. ............... 114
10. NAD Kinase and Phytochrome.. ............... 115
Appendix: On the Mechanism of the "High Irradiance Response" . 115
Suggested Further Reading. . . . . . . . . . . . . . . . . . . . .. 116
12th Lecture: Interaction between Phytochrome and Hormones. 118
1. Induction of Amylase by Plr . . 118
2. Induction of Peroxidase by Plr . . . . . . . . . . 121
Suggested Further Reading. . . . . . . . . . . . . 124
13th Lecture: The Double Function of Phytochrome in Mediating Anthocyanin
and Enzyme Synthesis . . . . . . . . . . . . . . . . . . . . . . . .. 125
1. Anthocyanin Synthesis. . . . . . . . . . . . . . . . . 125
2. Enzyme Synthesis . . . . . . . . . . . . . . . . . . . . . . 129
Appendix 1: Function of Plr in Ascorbic Acid Synthesis. . . . 130
Appendix 2: Induction of Nitrate-reductase in Corn Leaves. 130
Suggested Further Reading . . . . . . . . . . . . . . . . . . . . . .. 131
Contents VII
14th Lecture: Repression of Lipoxygenase Synthesis by Pt.: The Problem of Primary
and Secondary Differentiation . . . . . . . . . . . . . . . . . . . .. 132
1. Threshold Regulation of Lipoxygenase Synthesis: A Recapitulation 133
2. Some Experiments to Validate the Concept of the Double-action
Control Mechanism in Development. . . . . . . . . . . . . . . .. 133
3. Some Related Phenomena in Animal Physiology. . . . . . . . .. 138
4. Primary and Secondary Differentiation in Anthocyanin Synthesis. 138
5. Further Approaches to the Problem. . . . . . . . . . . . . . . .. 139
Suggested Further Reading . . . . . . . . . . . . . . . . . . . . . .. 140
15th Lecture: Light-mediated Flavonoid Synthesis: A Biochemical Model System of
Differentiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 141
1. The Starting Point . . . . . . . . . . . . . . . . . . . . . . . . .. 141
2. Phytochrome-mediated Anthocyanin Synthesis in the Mustard
Seedling as a Model System for Secondary Differentiation. . . .. 141
3. Flavone Glycoside Synthesis in Cell Suspension Cultures of Pars-
ley as a Model System for Primary and Secondary Differentiation. 144
4. Some General Remarks. . . . . . . . . . . . . . . . . . . . . . .. 146
Appendix: Phytochrome-mediated Anthocyanin Synthesis as a
Model System for Two-factor Analysis (Multiplicative Calculation). 147
Suggested Further Reading. . . . . . . . . . . . . . . . . . . . . .. 148
16th Lecture: Control of Distinct Enzymes (PAL, AO) in Different Organs of a
Plant (Mustard Seedling) . . . . . . . . . . . . . . . . . . . . . . .. 149
1. The Problem . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 149
2. The Advantages of the Experimental System Used for these In-
vestigations . . . . . . . . . . . . . . . . . . . . . . 149
3. PAL: Results and Conclusions .......... . 150
4. Ascorbate Oxidase (AO): Results and Conclusions. 152
Suggested Further Reading . . . . . . . . . . . . . . . 152
17th Lecture: Energetics of Morphogenesis. . . . . . . . . . . . . . . . . . . . .. 153
1. The Background . . . 153
2. The Hypothesis. . . . . . . . . . . . . . . . . . . . . . . . . . .. 154
3. General Conclusions. . . . . . . . . . . . . . . . . . . . . . . .. 155
4. Etiolation as an Adaptive Trait. . . . . . . . . . . . . . . 155
5. The Rapidity of Regressive (or Degenerative) Evolution. 155
6. A Final Speculation. . . . . . . . . . . . . . . . . . . . . 156
Suggested Further Reading . . . . . . . . . . . . . . . . . . 156
18th Lecture: Control of Plastogenesis by Phytochrome. . . . . . . . . . . . . .. 157
1. The System: Cotyledons of the Mustard Seedling. 157
2. The Aim of the Present Investigations. . . . . . . 158
3. Some Histological Data. . . . . . . . . . . . . . . 159
4. Control of Plastid Development by Phytochrome. 160
5. Control of Carotenoid Synthesis by Phytochrome. 161
6. Control of Galactolipid Biosynthesis by Phytochrome. 166
7. Control of Galactosyltransferase by Phytochrome. . . 168
8. Control of Glyceraldehyde-3-phosphate Dehydrogenase (GPD)
by Phytochrome . . . . . . . . . . . . . . . . . . . 169
9. Control of Chlorophyll Synthesis by Phytochrome. . . . . . . .. 170
VIII Contents
a) Basic Phenomena and the Leading Model at Present. . . . . .. 170
b) Feeding b-ALA to Mustard Seedlings. . . . . . . . . . . . .. 171
c) Control of Protochlorophyll (PChl) and Chlorophyll a (Chla)
Accumulation by Phytochrome. . . . . . . . . . . . . . . . .. 173
Suggested Further Reading . . . . . . . . . . . . . . . . . . . . . .. 175
Appendix: Phytochrome-mediated Control of Peroxisome Enzymes 175
Suggested Further Reading . . . . . . . . . . . . . 177
19th Lecture: Phytochrome and Flower Initiation. . . . . . . . 178
1. Definitions ............. . . . . . . . . 178
2. Involvement of Phytochrome . . . . . . . . . . . 179
3. Interaction between Phytochrome and Endogenous Rhythms. 179
4. The "Primary Action of Pf:' in Connection with Flower Initiation 183
5. Photoperiodic Effects on Vegetative Characteristics . . . . . . .. 183
Suggested Further Reading . . . . . . . . . . . . . . . . . . . . . .. 184
20th Lecture: Phytochrome and Seed Germination .................. 185
1. Operational Criteria for the Involvement of Pfr(ground in Seed
state)
Germination ............................. 185
2. The Inhibitory Effect of Long-term Far-red Light on Seed Germi-
nation . . . . . . . . . . . . . . . . . . . . . 185
3. Direct Phytochrome Measurements in Seed. 187
4. The "Mechanism" of Germination . . . . . 188
Suggested Further Reading . . . . . . . . . . . 189
21 Lecture: Examples of Blue-light-mediated Photomorphogenesis . . . . . . . . 190
st
1. Blue Light and the Phytochrome System . . . . . . . . . . . . . . 190
2. Light-dependent Carotenoid Synthesis in Fusarium aquaeductuum 190
3. Polarotropism in Filamentous Germlings of the Liverwort
Sphaerocarpus donnellii. . . . . . . . . . . . . . . . . . . . . . .. 191
4. The Light Growth Response in the Sporangiophore of the Fungus
Phycomyces . . . . . . . . . . . . . . . . . . . . . . . . 191
5. General Conclusions . . . . . . . . . . . . . . 192
6. Photomorphogenesis in Fern Gametophytes . 194
a) Basic Phenomena . . . . . . . . . . 194
b) The Problem of the Photoreceptor . 195
c) A Hypothesis . . . . . . . . . . 197
d) Test to Validate this Hypothesis. 197
e) Microscopic Data on Plastids . . 201
f) Data on RNA . . . . . . . . . . 201
g) Microscopic Data on Nuclei and Nucleoli. 202
h) Summary. . . . . . . . . . . . . . . . . . . 203
Suggested Further Reading . . . . . . . . . . . . 204
22nd Lecture: The Problem of Phototropism . . . . . . . . . . . 205
1. The Traditional View. . . . . . . . . . . . . . . 205
2. Phototropic Responses in a Unicellular System. 206
3. Phototropic Responses of the Hypocotyl . 207
4. Homeostasis and Integration . . . . . . . . . . 209
Suggested Further Reading . . . . . . 209
23rd Lecture: Genes and Environment ......................... 210
Contents IX
1. The Problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 210
2. The Principal Results of the Foregoing Lectures ......... . 211
3. Environmental Variability of Different Characteristics (or Traits) . 211
4. A Hypothesis to Explain the Phenomena Described in the Previous
Section .............................. . 212
5. Phenotypization of Genetic Information as a Two-step Process. 213
6. Future Topics for Research .................. . 214
Selected Further Reading . . . . . . . . . . . . . . . . . . . . . . . 215
24th Lecture: Epilogue: Science and Responsibility . 216
Suggested Further Reading . 226
Literature Cited 227
Subject Index .. 235
Use of Symbols
Unfortunately, there is no rigorously defined use of symbols and abbreviations in
experimental biology. The S.1. (Systeme International d'Unites), though formally
approved in 1960 by the Conference Generale des Poids et Mesures, is being accepted in
practice only slowly and sometimes even reluctantly. As a compromise the "General Rules
for Abbreviations" as defined in every January issue of Plant Physiology were followed in
the present text in cases where it seemed too premature to follow strictly the S.1. In
general dimensions and concentrations are denoted by brackets. In the following list those
abbreviations and symbols are put together which are not trivial and which are repeatedly
used in the text.
Symbol (or Abbreviation) Meaning
A(= O.D.) absorbance
LlA(=LlO.D.) change in absorbance
LlLIA(=LI (LlO.D.» change in change of absorbance
Act.D Actinomycin D
ALA o-amino-Ievulinic acid
AO ascorbate oxidase (EC 1.1 0.3.3.)
CAP chloramphenicol
d day
DGD digalactosyl diglyceride
E Einstein (= mole quanta)
E . cm-2 . S-1 quantum flux density
fr far-red light
GA3 gibberellic acid
GPD glyceraldehyde-3-phosphate dehydrogenase
h hour
HIR high irradiance response
LOG 1m lip oxygenase (EC 1.99.2.1.)
Ix (= ---mr) illuminance
M molar(= mole· liter-I)
MGD monogalactosyl diglyceride
mill minute
mole mole (a gram molecule)
f,l micro ... (= 10-6)
n nano ... (= 10-9)
nm nanometer (= 10-9 m)
XII Use of Symbols
p pico ... (= 10-12)
P phytochrome
P red absorbing form of phytochrome
r
Plr far-red absorbing form of phytochrome
[P] brackets in connection with phytochrome denote
concentration
PI/' some excited species of Plr
Plr (ground state) Plr in the ground state, that is, non-excited state
Ptotal = Ptot total phytochrome, that is, [PrJ + [Plr]
PAL phenylalanine ammonia-lyase (EC 4.3.1.5.)
r red light
second
T2I half-life
uv short wavelength ultraviolet « 300 nm)
W· cm-2 irradiance (light intensity)
X unknown reactant of phytochrome (Plr)
Some plants which are often mentioned in the text
buckwheat Fagopyrum esculentum Mach.
common male fern Dryopteris filix mas (1.) Schott
lettuce Lactuca sativa 1.
maIze, corn Zea mays 1.
(white seeded) mustard Sinapis alba 1.
oat A vena sativa 1.
pea Pisum sativum 1.
rye Secale cereale 1.