Table Of ContentDictyostelium discoideum
A Developmental System
William F. Loomis
Department of Biology
University of California at San Diego
La Jolla, California
ACADEMIC PRESS New York San Francisco London 1975
A Subsidiary of Harcourt Brace Jovanovich, Publishers
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Loomis, William F
Dictyostelium discoideum.
Bibliography: p.
1. Developmental biology. 2. Dictyostelium discoi
deum. I. Title. [DNLM: 1. Myxomycetes. QW180 L863d]
QP83.8.L66 593M17 74-27786
ISBN 0-12-456150-0
PRINTED IN THE UNITED STATES OF AMERICA
Preface
Dictyostelium discoideum has been attracting attention from an in
creasing number of biologists who have become aware of its unique
advantages as a model eukaryotic system in which to study a variety of
developmental problems. The organism lies in the transition zone between
major phylogenetic categories as shown by the fact that many botanists
consider it a lower plant while many zoologists consider it a lower
animal. It has many of the attributes and experimental advantages of
microorganisms but displays multicellular phenomena similar to those of
metazoans. Its rapid life cycle and small size make it convenient for
cytological studies, while its synchronous development allows biochemical
analyses.
The genetic and biochemical studies which, in recent years, have
begun to elucidate the physiological processes that underlie morpho
logical phenomena form the focus of this review. Earlier work has been
summarized in the excellent book of J. T. Bonner, "The Cellular Slime
Molds." Although many of the present studies do not provide conclusive
answers to the developmental problems, they better delineate the ques
tions and indicate fruitful approaches which can be pursued.
Biochemical processes which evolved several billion years ago in the
simplest unicellular organisms have been conserved down to present
day higher organisms to a surprising extent. Underneath the variety of
ix
χ Preface
morphological specializations of multicellular organisms, the pathways
of energy production and biosynthesis have remained almost unchanged.
The universality of the genetic code and the unique mechanism of
protein synthesis attest to the fact that once the necessary degree of
precision of gene expression was attained few further modifications
evolved.
Higher organisms came into existence about a billion years ago and
seem to have followed a pathway to specialization which often involved
using preexisting physiological functions in new combinations rather than
the evolution of completely new ones. Thus, a basic understanding of a
process in one organism often has much to say about related processes
in other systems.
I have attempted to put in focus most of the major studies on D.
discoideum. I have not tried to include all of the amazingly diverse facts
concerning this organism which have appeared in recent years. Many
preliminary observations cannot yet be incorporated into a coherent
fabric, and rather than attempting to be exhaustively complete, I have
tried to give the present approaches in a concise and useful form. For the
sake of continuity and brevity, studies on related slime molds have not
been included, although some species of the Acrasiales are described for
the purpose of comparison in Chapter 1.
The recent interest in development of D. discoideum has generated a
greatly increased flow of published works. Many of these repeat and
extend earlier work. Where possible the original papers have been re
ferred to in the text; however, it seemed cumbersome in this type of
book to exhaustively reference each observation discussed. Instead,
pertinent publications are indicated so that the reader can gain further
information on a point of interest. Excellent reviews of various aspects
of the development of D. discoideum have recently been published and
provide more complete referencing (see Garrod and Ashworth, 1973;
Newell, 1971; Bonner, 1971; Killick and Wright, 1974; Gregg and Bad-
man, 1973; and Sussman and Sussman, 1969). An effort has been made
to make the Bibliography on D. discoideum as complete as possible
to 1974.
I am indebted to my colleagues, Randall Dimond, Paul Farnsworth,
Richard Firtel, Steven Free, Hudson Freeze, and Ken Poff, for careful
reading of the manuscript and many helpful discussions. I am particularly
indebted to Dr. Paul Farnsworth for providing the illustrations for this
book. Studies in my laboratory have been supported by grants from the
National Science Foundation and the National Institutes of Health.
William F. Loomis
Chapter 1
The Life Cycle
An Overview
Dictyostelium discoideum is found in nature as a soil amoeba in forest
detritus. It was first discovered by Raper (1935) in the woods of North
Carolina but has since been found in similar ecological environments
throughout the world (Cavender and Raper, 1965a,b,c, 1968). The cells
feed on the bacteria of decaying fallen leaves and other matter and
divide by binary fission much like any other soil amoebae. However,
when the local environment is depleted of food source, a unique and
characteristic series of developmental events occurs which distinguishes
D. discoideum from less social organisms. The cells collect in large
streaming patterns to form groups containing up to 105 cells (Fig. 1.1).
These aggregates become integrated by deposition of a surface sheath
covering the whole mound. The aggregate topples over onto the surface
and migrates horizontally still surrounded by the sheath, and as such
is referred to as a pseudoplasmodium, grex, or slug (Fig. 1.2).
After a variable period of migration, the pseudoplasmodium stops
1
2 1. The Life Cycle
Fig. 1.1. Aggregation patterns. A shadowgraph of many cells aggregating to centers.
Each individual amoeba appears as a small white dot, while aggregation centers
appear as clear areas.
and the anterior tip moves vertically in preparation for the terminal
differentiations which form the fruiting body. At this point cells near
the tip of the mass begin to synthesize increased amounts of cellulose
A
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Fig. 1.2. A migrating pseudoplasmodium seen from above. The tapered anterior tip and the collapsed tube of surface sheath left
3
behind are clearly visible.
4 J. The Life Cycle
Fig. 1.3. Mature fruiting bodies. (A) Sori supported on tapering stalks. (B) Differ
entiated stalk cells (Nomarski optics); angular cellulose walls can be seen surround
ing the cells, which are enclosed in the stalk sheath. (C) Differentiated spores
(Nomarski optics).
A
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Fig. 1.4. Germinating spore. The emerging amoeba (A) can be seen escaping the spore case (S) through a longitudinal slit (L).
The specimen was fixed in 2% glutaraldehyde, postfixed in 1% osmium tetroxide and critical point dried from Freon (SEM).
5
6 1. The Life Cycle
forming a sheath within which the cells expand and vacuolize to form
the stalk. Once the stalk sheath makes contact with the underlying sup
port all further expansion results in extending the stalk vertically. The
peripheral cells are lifted up on the rising stalk which engulfs more
and more cells at its open upper end. The process has been compared
to a fountain running backward (Bonner, 1967). Once inside the stalk,
the cells expand and vacuolize lifting the whole mass up further. As
the mass rises, the peripheral cells begin to encapsulate and form the
apical sorus. When all of the cells have either been engulfed into the
stalk or have encapsulated to form spores, the formation of the fruiting
body is complete (Fig. 1.3).
Stalk cells are no longer viable after vacuolization but the spores
can remain viable through extended periods of dehydration, starvation,
and elevated temperature. When the spores are dispersed, they germinate
by splitting the spore case longitudinally and escaping as small but
normal amoebae (Fig. 1.4). The sequence of morphological stages is
shown schematically in Fig. 1.5.
GROWTH Q£)
GERMINATION
f SPORES
FRUITING Fig. 1.5. Life cycle of D. discoideum. Up
BODY
to 105 amoebae aggregate and form pseudo-
plasmodia. Fruiting bodies formed from such
aggregates are about 1-2 mm high and con
tain about 7 χ 104 ellipsoid spores.
The apparent selective advantage of this complex series of stages is
2-fold: to permit the dispersal of the cells from an area in which
they were starving and to provide a dormant stage to resist unfavorable
conditions. Impairment of either function would most likely be detrimen
tal to the cells' survival.
Synchronous development of up to 1011 cells can be achieved in the
laboratory by washing amoebae free of exogenous nutrients and deposit
ing them on filter papers soaked in a buffered salt solution (Sussman,
1966a). Under these conditions the cells proceed through the morpho
logical stages in 24 hours with greater than 95% synchrony. The develop
mental stages are shown in Figs. 1.6 and 1.7.
