AMKR. ZOOI.. 19:545-554 (1979).
Electron Microscopy and The Phylogeny of Green Algae and Land Plants
JEREMY D. PICKETT-HEAPS
Department of Molecular, Cellular and Developmental Biology, University of Colorado,
Boulder, Colorado 80309
SYNOPSIS. Electron microscopy of dividing green algal cells has demonstrated that there are
two quite separate phyletic lines in the L'lotrichales and Chaetophorales, groups that are
considered classically to have provided the progenitors of the green land plants. These
groups are distinguished by whether their mitotic spindle is "open" or "closed," and whether
their cytokinetic apparatus at telophase contains a persistent interzonal spindle in which the
microtubules are oriented perpendicular to the plane of cytokinesis (including the phragmoplast), or a "phycoplast," in which the microtubules are coplanar with the plane of
cytokinesis. The majority of genera of these two groups are related and have the closed
spindle and phycoplast, and so they are allied with the Volvocales, Chlorococcales, and the
Oedogoniales. A few genera from each group have the open spindle and the persistent
interzonal telophase spindle or the phragmoplast (the derivative of the persistent spindle),
as do the Conjugales (Zygnematales) and the Charales. That these latter plants are related
phyletically to the land plants is clearly demonstrated by the structure of their motile cells
(where formed): these are intrinsically asymmetric and possess a single band of cytoskeletal
microtubules, just as do the sperm cells of bryophytes, ferns, cycads, and the gyninosperni
tree, Gingko. In contrast, the motile cells of genera which have the phycoplast are derived
from a much more symmetrical (Chlamydomonad) cell-type with 2-4 bands of cytoskeletal
microlubules emanating from 2-4 basal bodies.
INTRODUCTION
Plant taxonomy utilizes many gross anatomical features in classification, and light
microscopy of plants and plant tissues has
been invaluable in such endeavors. The
light microscope suffers an inherent limitation in resolving power and this becomes
increasingly serious in attempts to investigate the internal morphology of plant cells.
When dealing with the vast range of small
unicellular algae presently known, as well as
with the simpler colonial (e.g., filamentous)
forms derived from them, the light microscope is often of limited value, and one
has to concentrate on other features of tax onomic value, for example, the biochemistry of their pigments, food reserves, and
cell walls (e.g., Bold, 1967:p. 11). However,
the micromorphology of such tiny cells,
while fascinating in its own right, has considerable value in their taxonomy and ultimately in understanding their phylogeny.
The author grateful!) acknowledges the grant support over a number of years from the Systematics
Section, N. S. F., which enabled much of this work to be
carried out.
The advent of electron microscopy has
changed the situation, providing us with a
plethora of data on cellular structure. Now
we are faced with the task of deciding which
of these data has taxonomic value, and how
much weight we should assign them in
comparison with data from more established procedures.
This paper concerns the way electron microscopy has fundamentally altered our
concepts of the phylogeny of green algae
and of their relationships to land plants.
That the land plants arose from green algae
cannot be disputed at this stage. Until a few
years ago, a relatively straightforward
evolutionary progression could be envisaged, whereby unicellular flagellates
evolved into simple filaments that in turn
became branched and acquired the ability
to form planar and more complex tissues as
well as differentiated cells such as rhizoids
(e.g., Scagel et al., 1965: p. 277). These
forms would have explored the possibilities
of heterotrichous growth, diploid life cycles, etc., as well as acquiring those characteristics (e.g., resistance to desiccation using
waterproof cuticles) necessary for adapta-
545
546
JEREMY D. PICKETT-HEAPS
tion to life out of water. The classical Ulotrichales and Chaetophorales (e.g., sensu
Fritsch, 1935) contain numerous extant
green algae which display, even now, combinations of such features. These forms
demonstrate facets of the evolutionary
progression that took place an unimaginably long time ago, soon after the Cambrian.
The electron microscope has now shown
that the situation is more complicated than
we had supposed. The relevant observations arose from the study of cell division,
an area of investigation that appeared at
first to have little, if any, relevance to
green-algal phylogeny.
This story starts with the paper by Johnson and Porter (1968) on cell division in the
well-known Chlamydomonas. Two observations are particularly important. First,
mitosis appears normal except that the nuclear envelope remains essentially intact
throughout mitosis. Such "closed" mitotic
spindles are commonplace in fungi, protozoa, and other algae, but they appear
more unusual in comparison to the "open"
spindles, portrayed in most textbooks, of
higher animal and higher plant cells.
Secondly—and, as it turned out later, most
importantly—cytokinesis is peculiar. The
cell cleaves, as do many other cells. More
unusual is the fact that daughter nuclei,
previously separated widely by the telephase spindle, soon come back close together. Meanwhile, a complicated array of
microtubules (MTs) appear between them.
These MTs all are oreinted in the plane of
cytokinesis, and the cleavage furrow passes
amongst these MTs to create two uninucleate daughter cells. An example of this
type of cytokinesis in the closely related Tetraspora is shown here (Fig. 1; Pickett-Heaps,
1973a).
My research group then became interested in several other groups of green
algae, particularly the taxonomically isolated Oedogoniales (Pickett-Heaps and
Fowke, 1969, 1970a,6; Pickett-Heaps,
19736, 1977). These strange and fascinating algae have a unique method of cell division, a unique zoospore and unique
oogamous sexual reproduction; taxonomically, they stand quite isolated in the green
algae. However, they have closed mitotic
spindles. During cytokinesis, the widely
separated daughter nuclei come close together, and then an array of MTs grows out
across the cell from between the nuclei,
oriented in the plane of the future wall.
Because of the peculiar way Oedogonium divides, it cannot cleave; instead, numerous
vesicles collect amongst the MTs. Later, this
diaphram-like array of MTs and vesicles is
moved to a different part of the cell, whereupon the vesicles fuse to give a crosswall.
Despite the peculiar nature of this cell division, it had obvious, if distant, affinities with
the mitotic and cytokinetic system of
Chlamydomonas.
We also began investigating many interesting members of the Chlorococcales, a
varied, natural grouping of green algae
that displays, amongst other traits, the
coenocytic or multinucleate tendency, in
which nuclear and cytoplasmic division
have become increasingly separated events.
Without exception, all diverse members of
the Chlorococcales studied have closed
spindles, and all have the same system of
cytokinetic MTs, oriented in the plane of
cell cleavage (e.g., Pickett-Heaps, 1970,
1972a; Marchant, \974a,b; Pickett-Heaps
and Staehelin, 1975). However, the
cytokinetic apparatus has undergone considerable evolution, since cytokinesis does
not necessarily follow mitosis. An example
shown here is of cleavage in a multinucleate
cell of Tetraedron (Fig. 2: Pickett-Heaps,
1972a). An extreme example of this separation of the two events is given by the waternet, Hydrodictyon, in which each tiny colonial, uninucleate vegetative cell grows
enormously while repeated waves of mitosis
produce thousands of nuclei in its cytoplasm (Marchant and Pickett-Heaps, 1970).
Only when some unknown trigger instigates the vegetative (or sexual) reproductive
cycle do the cleavage MTs appear, all at
once, throughout the cytoplasm between
the nuclei and under the vacuolar membrane (Marchant and Pickett-Heaps, 1971).
Complicated, ramifying furrows cleave the
cytoplasm into thousands of tiny uninucleate flagellated zoospores (or gametes)
after having isolated the vacuolar membrane. The basic cytokinetic system demonstrated in Chlamydomonas has been adapted
considerably in this and other genera (in-
GREEN ALGAL PHYLOGENY
1
FIG. 1. Tetraspora sp., a close relative of Chlamydo- furrow (cf) is passing between them through the
monas, undergoing cytokinesis. The daughter nuclei phycoplast (ph) whose microtubules are coplanarwith
have come together after telophase, and the cleavage the furrow. From Pickett-Heaps (1973a).
eluding Scenedesmus, Chlorella, Tetraedron,
Pediastrum, and others) to allow for their
more complicated life cycles. At this stage, I
decided that the system of cytokinetic MTs
was sufficiently prevalent to deserve its own
name, the "phycoplast" (Pickett-Heaps,
19726).
Meanwhile, Mattox and Stewart's group
were following cell division in the Ulotrichales, in which are found the simple,
uninucleate filamentous green algae. They
worked on organisms such as Ulothrix
(Floyd el al., 1971) as well as Sligeoclonium
(Floyd etal., 1972a) and Schizomeris (Mattox
etal., 1974), more complicated members of
the Chaetophorales. This latter group is
considered (e.g., by Fritsch, 1935) to be considerably more advanced than the Ulotrichales and to be the one which provided
the progenitors of the land plants. The results were consistent. With a few notable
exceptions, to be discussed soon, both Ulotrichales and Chaetophorales have closed
spindles and phycoplasts; the phycoplast is
used whether the cell actually divides using
a cleavage furrow (as in Chlamydomonas) or a
cell plate, the collection of vesicles, etc., that
fuse to form the new crosswall (as in
Oedogonium).
In summary, the closed mitotic spindle
and phycoplast are characteristic of the
Volvocales, Chlorococcales, Oedogoniales
and most (not all!) members of the Ulotrichales and Chaetophorales. Such consistency is entirely compatible with the classical view that these algal groups have a
common origin from a Chlamydomonas-Wke
progenitor (Scagel et al., 1965).
548
JEREMY D. PICKETT-HEAPS
FIG. 2. Tetrnedrnn bilrirlens. This cell is reproducing to clei, and now ihecvloplasm is cleaving upas ramifying
form ainospores (miniatures of the parental cell). It cleavage furrows (r/'l grow through phvcoplasts that
illustrates typical Ohloiococcalean behaviour: Mines- haw appealed between all the nuclei. From Picketlsive mitoses have produced numerous daughter nu- Heaps (1972«)
GREEN ALGAL PHYLOGENY
549
closed by a layer of sterile, protective tissue.
Thus, as Fritsch (1935) has suggested, they
Now the problem arises. If they arose seem to represent one remnant of those
from the Chaetophorales as was generally ancient lines of algal evolution that atassumed, one could predict that the land tempted colonization of the land. Whatever
plants, too, should divide using a closed their true nature, they have the open spinspindle and phycoplast. They do not. Their dle and the phragmoplast typical of higher
spindle is open, and the crosswall is formed plants (Pickett-Heaps, 1967).
in the well-known phragmoplast (illusAt this stage, I began to seek a simple
trated in every biology textbook), in which Ulotrichalean genus that has an open spinthe cytokinetic MTs are perpendicular to the dle that is persistent during telophase; by
plane of cytokinesis. Crosswall formation is analogy with Spirogyra, such a spindle could
via the cell plate {i.e., involving fusion of have permitted the evolution of the
massed vesicles, as in previous examples phragmoplast. I encountered one almost
cited). Is this difference significant? I be- immediately, the genus Klebsormidium
lieved it was somehow fundamentally im- (formerly, Hormidium). Independently and
portant, since the phycoplast had been so concurrently Floyd et al. (19726) were also
consistently preserved during the evolution investigating this genius, and they too
of several other algal groups. Botanists at stressed how different it is during cell divifirst could not attach much significance to sion in comparison to its supposedly very
this discrepancy, or else they considered the close relative Ulothrix. I concluded (Pickettevolution of the phragmoplast from the Heaps, 1972c) that this organism might
phycoplast a possibility (e.g., Stewart et al., provide the key to understanding Ulo1973).
trichalean evolution, probably being closer
Resolution of this matter commenced in affinity to the Conjugales than to most
with some earlier work we had done on the other members of the Ulotrichales. The
common Spirogrya (Fowke and Pickett- possibility that the Ulotrichales contain two
Heaps, 1969a,6), a member of another separate lines of evolution was raised in
group of green algae, the Conjugales (Zyg- this paper, and then formally presented
nematales). The spindle of Spirogyra is (Pickett-Heaps and Marchant, 1972). This
open; the nuclei are held far apart during new concept, based only on the nature of
cytokinesis, and no trace of a phycoplast the mitotic and cytokinetic apparatus, was
appears. Instead, a cleavage furrow grows strengthened by our subsequent discovery
inwards, and, most surprisingly, when it (Marchant and Pickett-Heaps, 1973) that
encounters the persistent telophase spindle the peculiar Ulotrichalean genus Coleoremaining between the daughter nuclei, a chaete also has an open spindle and a true
small phragmoplast appears that finishes phragmoplast.
off cytokinesis! This unexpected sequence
We then proposed splitting up the classiof events indicated how the phragmoplast cal Ulotrichales and Chaetophorales, so
might have arisen (Pickett-Heaps, 1969). that all those with the phycoplast were conMost importantly, to evolve a phragmoplast sidered to have common ancestry whose
probably required that the longitudinally affinities lay with the Volvocales, Chlororiented, interzonal MTs of the spindle ococcales, and Oedogoniales (Fig. 3). Those
persist throughout cytokinesis.
(few) genera with a persistent interzonal
The group Charales also provided addi- spindle and/or phragmoplast are considtional evidence. These plants are very com- ered derived from the lines of phylogenetic
plicated morphologically with many ad- advance that also gave rise to the bryovanced characteristics; some botanists ques- phytes, land plants and the Conjugales.
tions whether they should be considered Our proposal was greeted, not surprisinggreen algae at all. They display, for exam- ly, with considerable skepticism, and furple, advanced oogamous reproduction dur- ther supporting evidence was urgently
ing which the reproductive cells are en- needed. It was soon forthcoming.
THE PROBLEM OFTHE PHRAGMOPLAST
Some PRASINOPHYTES
(eg. Pyramimonas)
FLAGELLATE WITH THE
PERSISTENT INTERZONAL
SPINDLE AT TELOPHASE
ARCHETYPAL
FLAGELLATE
(Pedinomonad - type?)
EVOLUTION
OF THE
PHYCOPLAST
\
CHLAMYDOMONADTYPE PROGENITOR
CONJUGALES
CHARALES
/
-4- (Evolution of the
^
^ a . t )
\ Some ULOTRICHALES
COLEOCHAETACEAE
(eg. Klebsormid/um)
CHAETOSPHAERIDICEAE
BRYOPHYTES and
HIGHER LAND PLANTS
Some PRASINOPHYTES ->
(eg. Platymonas)
VOLVOCALES
(inc. Tetrasporales)
CHLOROCOCCALES
PHYCOPLAST-FORMING
ORGANISMS
Some ULOTRICHALES
and CHAETOPHORALES
OEDOGONIALES
FIG. 3. Diagrammatic summary o( the evolutionary relationships of several green algal groups, and their affinities with the bryophytes and land
plants. These relationships are deduced primarily from the ultrastructure of their mitotic spindle, cytokinetic apparatus and motile cell (zoospore
and/or gamete), where formed. Modified from Pickett-Heaps and Ott (1974).
GREEN ALGAL PHYLOGENY
551
phylogeny applies well here; for example,
when Ulothrix forms zoospores, it appears
to recreate the cell type from which it origiThe organization of the Chlamydomonas nally evolved. Furthermore, the arrangecell, and particularly of its flagellar ap-* ment of organelles within the cell of such
paratus and MT cytoskeleton, illustrates filamentous forms often is asymmetric: the
the structure of the motile cell of many chloroplast is on one side of the cell, the
other green algae. It is basically bilaterally nucleus and centrioles on the other. This
symmetrical, as is its flagellar apparatus in- arrangement can be attributed to the origin
serted in one end. The two flagella (Ringo, of such filaments from unicellular flagel1967) are attached to two basal bodies that lates laterally stacked side by side, the only
are interconnected in a V-arrangement by colonial arrangement of such unicells that
sets of striated fibers. There are usually two permits the filamentous construction (see
more, non-functional basal bodies lying be- discussion in Pickett-Heaps, 1976).
tween these two and not connected to
In summary, therefore, those green
flagella. Four sets of "rootlet" MTs, in an algae that display their phylogenetic
X-arrangement, radiate outwards under affinities by utilization of the phycoplast for
the cell membranes from the area occupied cytokinesis also all have motile cells whose
by the basal bodies; these MTs appear to organization is basically similar, derived
function as cytoskeletal elements transmit- from a Chlamydomonas-Yike cell. Even the
ting the forces of flagellar motion through- huge, multiflagellated zoospore of the
out the cell body. The MTs at the base of the Oedogoniales can be explained in terms of
rootlets are arranged precisely; and their an increasing replication of the alternating
number, organization, and the ancillary basal-body/rootlet units that form a fourstructures associated with them, are charac- membered flagellar ring in quadriflagellate
teristic for any given species or genus.
unicells such as Carteria (Ringo, 1967).
This basic cellular architecture, with
In stark contrast are the sperm of the
numerous minor variations, is consistently Charales and the bryophytes. These sperm
encountered amongst the motile cells of the are highly differentiated and coiled, with
Volvocales, Chlorococcales, and many nucleus, mitochondria, and plastids linUlotrichales (Pickett-Heaps, 1975a,6). For early arranged along a single flat band of
example, in quadriflagellate unicells such as cytoskeletal MTs. The two basal bodies are
Carteria and Polytomella, all four basal bodies inserted skew at one end of the band, one
appear functional, arranged either as four behind the other. The bryophyte sperm
equivalent basal bodies, or two sets of two also possess a complex "Multi-LayeredV-shaped groups at right angles, one be- Structure" (MLS) of unknown function behind the other. The complexity of the root- tween the basal bodies and end of the MT
let MT system varies considerably; nor- band (e.g., Carothers, 1973, 1975; Kreitner
mally again, the four rootlets are either all and Carothers, 1976). Instead of an MLS,
the same, or else they form two sets of two Chara possesses a dense, featureless body in
types, alternating around the flagellar base. its place (Pickett-Heaps, 1968). The sperm
The zoospores of the Chlorococcales and cells of other land plants display these feamost Ulotrichales are clearly of this general tures, although they (like the motile zoopattern (Moestrup, 1978). Gametes of green spore and sperm of the Oedogoniales) have
algae have hardly been studied, except become highly multiflagellated. Enlargethose of Chlamydomonas where they are simi- ment from the basically asymmetric flagellar to the organization of vegetative cells but lar apparatus gives rise to a spiral (instead
with a few additional structures involved in of a circular ring) of increasing length; the
fertilization. Gametes of Hydrodictyon dis- increasingly numerous basal bodies are asplay similar specialized features (compare sociated with an enlarging MLS and an inFriedmann et al., 1968 with Marchant and creasingly large, single band of MTs (e.g.,
Pickett-Heaps, 1972).
Duckett, 1973, 1975; Norstog, 1974; Robbins and Carothers, 1978). This evolution
The principal of ontogeny recapitulating
THE MOTILE CELLOF GREEN ALGAE AND LAND
PLANTS
552
JEREMY D. PICKETT-HEAPS
of the flagellar apparatus can be seen by
comparison of the sperm of Marsilea (the
waterfern), ferns, cyads, and, the ancient
tree Gingko. Norstog (1974) estimates that
the sperm cell of Zamia (a cycad) contains
about 10,000 basal bodies while its single
cytoskeletal band contains around 60,000
MTs. Again, in the structure of their motile
cells, we can trace a common phylogenetic
ancestry of these organisms. During cell division, these plants have the open spindle
and the phragmoplast.
With this discussion, a test of our proposal is now obvious. The Conjugales never
have flagellated motile cells, but undergo
their characteristic sexual reproduction via
conjugation utilizing amoeboid gametes.
However, the "Ulotrichalean" genus Klebsormidium does form both motile zoospores
and gametes. Examination of the zoospore
of Klebsormidium with electron microscopy,
gave us the evidence needed (Marchant et
al., 1973). Not only is the zoospore asymmetric, containing a single flat band of
cytoskeletal MTs with the flagella asymmetrically inserted at one end, but it even has
the MLS! The zoospore of Coleochaete is
similar, even to the possession of the MLS
(Pickett-Heaps and Marchant, 1972). Such
a result is entirely predictable from the new
phylogenetic scheme (Pickett-Heaps,
1975a); it cannot be explained from more
classical phylogenies. The zoospore of
Chaetospheridium (Moestrup, 1974) also possesses the MLS and single band of MTs, but
its cell division remains to be investigated.
Further supportive evidence came from
another, unexpected quarter. In studying
two equivalent but separate enzymes associated with plant microbodies, glycolate
dehydrogenase and glycolate oxidase, Frederick et al. (1973) discovered that organisms with the phycoplast display dehydrogenase activity. Those algae that we derived from the phylogenetic lines leading to
the higher land plants have glycolate
oxidase, the enzyme characteristic of
higher plant microbodies. An earlier observation by Stewart et al. (1972) that the microbody of Klebsormidium behaved cytochemically like those of higher plants (in
contrast to those of several other green
algae) now made sense.
Three separate lines of evidence, therefore, now confirm that the affinities of
many groups of green algae are more complex than we had supposed. In particular,
the land plants arose from phylogenetic
lines separate from those that gave rise to
most of the modern Ulotrichales. More
subtle variations uncovered in mitotic and
cytokinetic systems have generated further
phylogenetic data that is more difficult to
assess at this stage and that need not be
considered here. For a comprehensive review, see Pickett-Heaps (1975ft). Much remains to be done in clarifying these matters
further. Numerous extant algae that I have
not mentioned here, deserve detailed ultrastructural and biochemical investigation,
particularly the heterogeneous collection of
flagellates lumped together as the group
Prasinophyceae and the numerous large
coenocytic forms in the Siphonales. The
taxonomy of several algal groups will have
to be overhauled, a task already initiated by
Stewart and Mattox (1975). Many intriguing questions also arise. For example, why
were the phragmoplast-containing lines
successful in colonizing the land, and why
do they now appear relatively uncompetitive in more characteristic algal environments? How did the phycoplast arise originally? Was there one stock ancestral to all
green algae? Such is the progress of modern biology and the appearance of investigative methods undreamed of a short time
ago that we may hope that such questions
do not remain unanswerable.
REFERENCES
Bold, H.C. 1967. Morphology; of plants. Harper & Row,
New York.
Carothers, Z. B.. 1973. Studies of spermatogenesis in
the Hepaticae. IV. On the blepharoplast of Blasia.
Amer.J.Bot. 60:819-828.
Carothers, Z. B. 1975. Comparative studies on spermatogenesis in bryophyles. In J. G. Duckett and P.
A. Racey (eds.). The biology of the male gamete, pp.
71-84. Academic Press, New York.
Duckett, J. G. 1973. An tiltrastructural study of the
differentiation of the spermatozoid of Equisetum. J.
CellSci. 12:95-129.
Duckett, J. G. 1975. Spermatogenesis in pteridophytes. In J. G. Duckett and P. A. Racey (eds.), The
biology oj the male gamete, pp. 97-128. Academic Press,
New York.
GREEN ALGAL PHYLOGENY
553
Floyd, G. L., K. D. Stewart, and K. R. Matlox. 1971.
Hagellar apparatus in green algae and other
Cytokinesis and plasmodesmaia in L'lothrix. J.
chlorophyll a and 6-containing plants. BioSystems
Phycol. 7:306-309.
10:1 17-144.
Floyd, G. L., K. D. Stewart, and K. R. Mattox. 1972o. Norstog, K. 1974. Fine structure of the spermatozoid
Comparative cytology of L'lothrix and Stigeoclonium. of Zamia: The vierergruppe. Amer. J. Bot. 61:449J. Phycol. 8:68-81.
456.
Floyd, G. L., K. D. Stewart, and K. R. Mattox. 19726. Pickett-Heaps, J. D. 1967. Ultrastructure and differCellular organization, mitosis, and cytokinesis in the
entiation in Chara. II. Mitosis. Aust. J. Biol. Sci.
Ulolrichalean alga, Klebsormidium. J. Phycol. 8:176- 20:883-894.
184.
Pickett-Heaps, J. D. 1968. Ullrastructure and differFowke, L. C. and J. D. Picketi-Heaps. 1969n. Celldivientiation in Chara fibrosa. IV. Spermatogenesis.
sion inSpirogyra. I. Mitosis. J. Phycol. 5:240-259.
Aust. J. Biol. Sci. 21:655-690.
Fowke, L. C. and J. D. Pickett-Heaps. 1969*. Cell divi- Pickett-Heaps, J. D. 1969. The evolution of the mi tot ic
sion in Spirogyra. II. Cytokinesis. J. Phycol. 5:273apparatus: An attempt at comparative ultrastruc281.
tural morphology in dividing plant cells. Cytobios
Frederick, S. E., P. J. Gruber, and N. E. Tolbert. 1973.
3:257-280.
The occurrence of glycolate dehydrogenase and Pickett-Heaps, J. D. 1970. Mitosis and autospore forglycolate oxidase in green plants: An evolutionary
mation in the green alga Kirchneriella lunaris. Protosurvey. Plant Physiol. 52:318-323.
plasma 70:325-348.
Friedmann, I., A. L. Colwin, and L. H. Colwin. 1968. Pickett-Heaps, J. D. 1972«. Cell division in Tetraedron.
Fine-structural aspects of fertilization in Chlamydo- Ann. Bot. 36:693-701.
monas reinhardi. J. Cell Sci. 3:115-128.
Pickett-Heaps, J. D. 19726. Variation in mitosis and
Fritsch, F. E. 1935. Structure and reproduction oj the algae,cytokinesis in plant cells; its significance in phylogVol. I. Cambridge University Press.
eny and evolution of ultrastructural systems. Cyiobios 5:59-77.
Johnson, U. G. and K. R. Porter. 1968. Fine structure
of cell division in Chlamydomonas reinhardi. J. CellPickett-Heaps, J. D. 1972r. Cell division in KlebsorBiol. 38:403-425.
midium subtilissimum (formerly Ulothrix subtilissima),
and its possible phylogenetic significance. Cyiobios
Kreitner, G. L. and Z. B. Carothers. 1976. Studies of
6:167-183.
spermatogenesis in the Hepaticae. V. Blepharoplast
development in Marchantia polymorpha. Amer.J. Bot.Pickett-Heaps, J. D. 1973rt. Cell division in Tetraspora.
63:545-557.
Ann. Bot. 37:1017-1025.
Marchant, H.J. 1974a. Mitosis, cytokinesis and colony Pickett-Heaps, J. D. 19736. Cell division inBulbochaete.
I. Divisions utilizing the wall ring. J. Phycol. 9:408formation in Pediastrum boryanum. Ann. Bot.
420.
38:883-898.
Marchant, H.J. 19746. Mitosis, cytokinesis and colony Pickett-Heaps, J. D. 1975o. Structural and phylogeneformation in the green alga Sorastntm. J. Phycol.
tic aspects of microtubular systems in gametes and
10:107-120.
zoospores of certain green algae. In J. G. Duckett
and P. A. Racey (eds.). The biology of the male gamete,
Marchant, H.J. and J. D. Pickett-Heaps. 1970. Ultrastructure and differentiation of Hydrodictyon re- pp. 37-44. Acad. Press, New York.
ticulatum. I. Mitosis in the coenbium. Aust. J. Biol. Pickett-Heaps, J. D. 19756. Green algae. Sinauer Assoc,
Sci. 23:1173-1186.
Stamford, Conn.
Marchant, H.J. and J. D. Pickett-Heaps. 1971. Ultra- Pickett-Heaps, J. D. 1976. Cell division in eucaryotic
structure and differentiation of Hydrodictyon re- algae. BioScience 26:445-450.
ticulatum. II. Formation of zooids within the Pickett-Heaps, J. D. 1977. Cell division and evolution
of branching in Oedocladium (Chlorophyceae).
coenobium. Aust, J. Biol. Sci. 24:471-486.
Cytobiologie 14:319-337.
Marchant, H.J. and J. D. Pickett-Heaps. 1972. Ultrastructure and differentiation of Hydrodictyon re- Pickett-Heaps, J. D. and L. C. Fowke. 1969. Cell division in Oedogonium. I. Mitosis cytokinesis and cell
ticulation. IV. Conjugation of gametes and the
elongation. Aust.J. Biol. Sci. 22:857-894.
development of zygospores and azygospores. Aust.
J.Biol. Sci. 25:279-291.
Pickett-Heaps, J. D. and L. C. Fowke. 1970n. Cell division in Oedogonium. II. Nuclear division in 0. carMarchant, H.J. and J. D. Pickett-Heaps. 1973. Mitosis
and cytokinesis in Coleochaete scutata. J. Phycol. diacum. Ausl. J. Biol. Sci. 23:71-92.
10:461-471.
Pickett-Heaps, J. D. and L. C. Fowke. 19706. Cell division in Oedogonium. III. Golgi bodies, wall structure
Marchant, H.J..J. D. Pickett-Heaps, and K.Jacobs.
and wall formation in O.cardiacum. Aust.J. Biol. Sci.
1973. An ultrastructural study of zoosporogenesis
23:93-113.
and the zoospore of Klebsormidium flaccidum.
Cytobios 8:95-107.
Pickett-Heaps, J. D. and H. J. Marchant. 1972. The
phylogeny of the green algae. A new proposal.
Mattox, K. R., K. D. Stewart, and G. L. Floyd. 1974.
The cytology and classification of Schizomeris leib- Cytobios 6:255-264.
leinii. I. The vegetative thallus. Phycologia 13:63-70. Pickett-Heaps, J. D. and D. VV. On. 1974. Cell structure
Moestrup, O. 1974. Ullrastructure of the scaleand division in Pedinomonas. Cytobios 11:4 1-58.
covered zoospores of the green alga Chaetosphae- Pickett-Heaps, J. U. and L. A. Staehelin. 1975. The
ridium, a possible ancestor of the higher plants and
ultrastructure of Srenedetmiis (Chlorophyceae). II.
bryophytes. Biol. J. Linnean Soc. 6:11 1-125.
Cell division and colony formation. J. Phycol.
11:186-202.
Moestrup, O. 1978. On thephylogenetic validity of the
554
JEREMY D. PICKETT-HEAPS
Ringo, D. L. 1967. Flagellar motion and fine structure _
54:431-434.
of the flagellar apparatus in Chlamydomonas. J. Cell Stewart, K. D., K. R. Mattox, and G. L. Floyd. 1973.
Biol. 33:543-571.
Mitosis, cytokinesis and distribution of plasmodesRobbins, R. R. and Z. B. Carothers. 1978. Spermata and other cytological characteristics in the
matogenesis in Lycopodium: The mature sperUlotrichales, Ulvales and Chaetophorales —
matozoid. Amer.J. Bot. 65:433-440.
phylogenetic and taxonomic considerations. J.
Scagel, R. F., R. J. Bandoni, G. E. Rouse, W. B.
Phycol. 9:128-141.
Schofield.J. R. Stein, and T. M. C. Taylor. 1965. An
Stewart, K. D. and K. R. Mattox. 1975. Comparative
evolutionary survey of the plant kingdom. Wadsworth
cytology, evolution and classification of the green
Publishing Co., Belmont, Calif.
algae with some consideration of the origin of other
Stewart, K. D., G. L. Floyd, K. R. Mattox, and M. E.
organisms with chlorophylls a and b. Bot. Rev.
Davis. 1972. Cytochemical demonstration of a single
41:104-135.
peroxisome in a filamentous green alga. J. Cell Biol.