The evolution and biological significance of seeds

T. A . STEEVES
Department of Biology, University of Saskatchewan, Saskatoon, Sask., Canada S7N OW0
Received January 11, 1983

STEEVES,
T. A. 1983. The evolution and biological significance of seeds. Can. J. Bot. 61: 3550-3560.
No evolutionary event in the colonization of the land by vascular plants is of greater significance than the appearance of the
seed habit. What apparently began as an adaptation enhancing sexual reproduction in the absence of external free water has
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assumed a far broader importance in terms of survival and dispersal. The essential features of the seed habit are identified in
relation to heterospory, megaspore retention, and endosporic gametophyte development and approaches to the seed habit by
nonseed plants are reviewed. Seeds first appear in the fossil record of the Late Devonian Period and, in diverse forms and sizes,
constitute a significant component of Carboniferous fossil floras. The rise to dominance of plants of gymnospermous affinity in
the early Mesozoic and the appearance and rapid adaptive radiation of the angiosperms are discussed in relation to the significance
of the seed habit. The structure and development of modem gymnosperm and angiosperm seeds are compared, and the
contrasting patterns of embryogenesis in these two types of seeds are interpreted in terms of the relationship between the embryo
and its nutritive support system.

STEEVES,
T. A. 1983. The evolution and biological significance of seeds. Can. J. Bot. 61: 3550-3560.
I1 n'y a aucun aspect plus important de la colonisation de la terre fenne par les plantes vasculaires que 1'Cvolution de la graine.
D'abord une adaptation facilitant la reproduction sexuCe en absence d'eau ambiante, les graines ont assume un r8le beaucoup plus
vaste pour la survie et la dissemination. L'auteur signale les traits reproductifs des plantes h graines a l'Cgard de l'hCtCrosporie, de
la rCtention de la megaspore et de l'endoprothallie et resume quelques phknombnes semblables parmi les cryptogames. Les plus
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anciennes graines fossilises se trouvent dans les strates devoniennes superieures et elles sont abondantes et variees dans les flores
carbonifbres. L'essor puis la dominance des plantes gymnospennes t8t dans l'bre mCsozoi'que et l'apparition et 1'Cvolution rapide
des angiospennes un peu plus tard sont discutCs par rapport h l'importance de la reproduction au moyen de graines. La structure et
le dCveloppment des graines des gymnospermes et des angiospennes modernes sont compares et les embryogenies divergentes
des deux categories de graines sont interprCtCes en rapport avec la relation entre l'embryon et son systbme nutritif.

Introduction worldwide fauna. Probably the most recent species to

Most botanists would agree that no evolutionary event
in the conquest of the land by vascular plants is of greater
significance than the appearance of the seed. Since
Mesozoic times the earth's land surfaces have been
dominated by plants which reproduce by means of seeds
to the near exclusion of other vascular plants. While it is
true that the living gymnosperms do not equal either the
modem lycopods or the ferns in numbers of species,
their contribution to the terrestrial vegetation vastly
outweighs that of these non-seed-bearing plants. More-
over, in the angiosperms we confront the supremely
successful land plants from all points of view. The
evolution of seeds, which seems to have begun as a
device facilitating sexual reproduction on dry land, has,
in the flowering plants, been adapted to a variety of other
functions including a mechanism for dispersal par
excellence, a means of surviving periods unfavorable for
growth, and even, in the case of agamospermy, a device
for asexual propagation.
Beyond this, the impact of the seed habit upon other
organisms has been enormous. One need only mention
the coevolution of several insect groups and the angio-
sperms which they pollinate to affirm this point. More-
over the birds, mammals, and insects which have
evolved as seed eaters are an important part of the
establish an intimate relationship with seed-bearing
plants is Homo sapiens, for whom seeds provided the
foundation of a crucial phase of cultural evolution, the
invention of agriculture.
In this symposium several specialists consider aspects
of seed biology which are at the focus of current research
interest. The purpose of this introductory paper is to set
the stage for these presentations by giving an overview
of the seed and the seed habit from the long-term
perspective of vascular plant evolution.
Seeds and the seed habit
Until the middle of the 19th century botanists regard-
ed the seed plants as being relatively open about their
sexual habits; the pollen contributed the male element
which was by various means conveyed to the female
element in the ovule with the object of fertilization. The
seed plants were accordingly known as phanerogams
(phaneros, visible). On the other hand the cryptogams
(cryptos, hidden) seemed to conceal their sexual activit-
ies, if indeed they had any, and hence their name. The
brilliant deductions of Hofmeister (1862) of course
changed all of that. He revealed the sexuality of the
"cryptogams" by demonstrating their two-phase life
cycle, the gametophyte generation of which is obviously
 STEEVES
sexual. He also demonstrated that the "phanerogams"
follow the same alternating pattern of generations but, in
a manner which contradicts their name, obscure their
fusion processes to such an extent that modem ultra-
structural studies have only recently begun to elucidate
them.
It is generally accepted today that the seed habit is a
derivative of free-sporing heterospory, that is, a condi-
tion such as is found in modem Selaginella in which the
spores which produce male and female gametophytes
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are freely shed but differ markedly in size. This view has
been challenged from time to time (Thomson 1934;
Doyle 1953) on the grounds that in some modem seed
plants there is often little or no difference in size between
microspores and megaspores. However, Devonian pal-
aeobotanical studies appear to have resolved this ques-
tion once and for all. In the epochs preceding the first
amearance of seeds in the fossil record there was a
steady increase in the occurrence of heterospory and in
the differentiation between the two spore types (Chal-
oner 1970; Pettitt 1970). Heterospory clearly precedes
the seed habit in the fossil record. Moreover, the oldest
known seeds shown an unmistakable structural relation-
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ship to typical megaspores and megasporangia.
The phenomenon of heterospory is in itself a matter of
some interest and there is speculation as to its original
significance. At the genetic level, the guaranteed separa-
tion of sexes may be looked upon as favoring recom-
bination and thus having selective advantage. Such a
separation, however, may also be achieved by hetero-
thallism with no spore modification other than sex
determination. The size difference between microspores
and megaspores would seem to have an entirely different
significance in terms of nutrition. The megaspore,
which gives rise to the female gametophyte, can be
supplied with extensive reserves which will ultimately,
after fertilization, nurture the developing sporphyte,
.
while the micros~ore. . the work of which is done with the
release of male gametes, requires only minimal nutri-
tion. This then becomes a matter of efficiency and
economy; the energy resources are placed only where
they are needed. It is also of interest that in all modem
free-sporing heterosporous species the gametophytes
are endosporic; that is, the gametophyte develops
completely or almost completely within the confines of
the protective spore wall and thus is relieved of any
significant energy dependence upon the external en-
vironment. This pattern was certainly an early addition
to the evolution of heterospory, but the fossil record
does not reveal at what stage it actually appeared (Pettitt
1970).
The transition from the free-sporing heterosporous
condition to the seed habit in principle involves a
relatively simple change, but it is difficult to visualize
the intermediate stages of its establishment. Structurally
355 1
a seed (or ovule) is a megasporangium which contains a
megaspore which is not released and is in turn surround-
ed by some sort of protective integument. In our
ordinary understanding of a seed there is only one
functional megaspore, indeed usually only one spore
tetrad of which three members abort. However, it cannot
be assumed that this reduction to one megaspore was
necessarily completed before the nonshedding of mega-
spores was achieved. There may have been cases in
which multiple megaspores were retained. The fossil
record does not suggest this, but the absence of evidence
does not provide a final answer (Pettitt 1970).
It is necessary at this point to consider the seed in the
context in which it occurs, the seed habit. The ovemd-
ing biological significance of the seed habit, as opposed
to free-sporing heterospory, is that the process of
fertilization occurs in situ without the need for an
external fluid medium for the transfer of male gametes.
In the seed habit this is accomplished by the transfer of
microspores (in modem forms at least with partially
developed male gametophytes) to the attached mega-
sporangium with its retained megaspore and female
gametophyte. By various mechanisms subsequent to the
transfer, the male gamete reaches the female gamete
without having to swim or float through an external
watery medium. This represents the achievement of a
truly terrestrial mode of sexual reproduction, the ulti-
mate emancipation from the aquatic ancestry of the land
plants. In functional terms it is comparable with the
parallel development of internal fertilization among the
land vertebrates and arthropods. In the present flora of
the earth, plants with the archaic "cryptogamic" pattern
of reproduction are, like the amphibians, successful
only where water is abundant at least periodically, or
else they rely heavily upon vegetative mechanisms of
propagation. It is interesting to recall what has happened
here. Originally the spore, with its resistant wall was,
and in living vascular cryptogams remains, an agent of
dispersal. In seed plants this function is performed by
the seed and the old free-sporing mechanism has been
adapted to a new role, that of gamete transfer.
This raises some intriguing questions about certain
plants not in the seed-plant lineage which seem to have
achieved the seed habit independently. The fossil record
of the Carboniferous contains abundant examples of
Lepidocarpon and Achlamydocarpon, produced by
arborescent lycopods, in both of which a single large
megaspore was retained within a megasporangium
which in turn was attached to a sporophyll. In Lepido-
carpon there was the further parallelism that a kind of
integument was formed from lateral portions of the
sporophyll with a slitlike "micropyle" at the top.
However, it now appears that the structural parallelism
was not matched by a functional one (Phillips 1979). Far
from being an adaptation to terrestrial fertilization, the
 3552 CAN. 1. BOT. VOL. 61, 1983
sporophyll-sporangium unit is now thought to have
been a boatlike dispersal device in a swamp environment
with abundant standing water and fertilization is be-
lieved to have occurred in the water. It is debatable
whether this can be called an example of the seed habit,
but the dispersal unit was certainly seedlike in structure.
This interpretation, however, has been questioned by
Thomas (1981), who considers it probable that micro-
spore transfer to the megasporangium occurred before
the sporangium-sporophyll unit was shed.
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T h e origin of seeds
The evolutionary lineage which led to the true seed
plants (gymnosperms and angiosperms) clearly emerged
by the Late Devonian Period, a fact which has been
recognized since 1960 when Charles Beck demonstrated
that Archaeopteris, previously thought to be a fern, in
fact consisted of the branches and foliage of a treelike
plant with conifer-type secondary xylem (Beck 1960).
This discovery led to the naming of the progymno-
sperms, precursors of the gymnosperms but, by defini-
tion, themselves not seed plants. Since that time the
group has been enlarged as a result of both new
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discoveries and the reinterpretation of already known
fossil plants (Bonamo 1975; Beck 1976a; Stewart
1981). Many, perhaps most, of these plants were
heterosporous. More recently structures which can only
be interpreted as primitive seeds have also been extrac-
ted from Upper Devonian rocks and are believed, by
association, to have been borne by some of the plants of
this type, possibly even by species of Archaeopteris
itself. However, by strict definition any such plants
which produced seeds would not be progymnosperms,
but primitive gymnosperms.
The original, and most famous, of these early seeds is
Archaeosperma arnoldii, discovered by Pettitt and Beck
(1967, 1968) in material from northern Pennsylvania.
The seeds were borne in pairs partially surrounded by a
kind of cupule and the cupules were in turn paired. The
individual ovule consisted of a megasporangium (or
nucellus as it might now be called) surrounded by an
integument and containing a megaspore tetrad, three
members of which are believed to have been nonfunc-
tional. Unlike the situation in modem seeds plants, the
tetrad had a tetrahedral rather than linear arrangement. It
has been assumed that in Archaeosperma pollination
occurred in situ so that we have here an example of the
seed habit, not just a seedlike structure. Unfortunately
the distal end of the nucellus was not well enough
preserved to permit any objective conclusions about the
method of pollen reception. However, very recently
(Gillespie et al. 1981) even older and as yet unnamed
seeds have been described from fossil beds in West
Virginia in which the apex of the nucellus is seen to have
been developed into a tubelike salpinx connected to a
pollen chamber. There can be little doubt that we are
dealing here with pollination as the term is understood
today. There remains of course the intriguing question
of how pollination evolved from the free-sporing condi-
tion, what were the intermediate stages and what
advantage did they confer which might have led to their
selection and further elaboration?
As we move into the Carboniferous, seeds become
commonplace in the fossil record and a substantial
diversity is to be found. The Early Carboniferous seeds
are assigned for the most part either to the seed ferns
(pteridosperms) or to the cordaites of the coniferophyte
e v o l u t i o ~line. Basically there appear to have-been
trends leading to the fusion of integumentary lobes and
modification of the distal region into a well-defined
micropyle (Andrews 1963). In fact, the Early Carbonif-
erous Genomosperma kidstonii is actually more primi-
tive in construction than Archaeosperma in that the
"integument" consists of eight separate filaments un-
fused to the base. It has been suggested that these
changes are associated with enhanced protection from
both desiccation and foraging insects and also with more
efficient pollination. On the assumption, generally
accepted, that the chief pollen transfer agent was wind,
Niklas (198 1) has studied the aerodynamic properties of
scale models of several Early Carboniferous seeds and
also the behaviour of scale models of primitive pollen
grains in flowing air. These studies seem to show the
progressive enhancement of wind pollination in the
more highly evolved seeds. However, Rothwell and
Taylor (1982) have pointed out some technical flaws in
these experiments which caution against unqualified
acceptance. Moreover, the role of insects as pollinators
cannot be ruled out, particularly in certain cases in
which the pollen gain> are known to have been very
large (Taylor and Millay 1979; Taylor 1982).
The close relationship between the seed habit and
free-sporing heterospory is shown with particular clarity
in the evolution of pollen. In the lower, free-sporing
vascular plants spore germination occurs by a cracking
open along the trilete or monolete lines of contact with
the other spores of the tetrad. This is called the proximal
face of the spore in reference to its position in the tetrad.
By contrast, in the pollen of modem seed plants,
germination occurs on the opposite or distal face or
equatorially, by means of an area of reduced wall
thickness (colpus or pore) and it is from this region that
the ~ o l l e tube
n exits. While it is difficult to derive a "
ereat
d e i of detailed information on matters of this sort from
fossil material, some interesting observations have been
made by careful study of the wall structure of pollen
grains found within the ovules of Palaeozoic gymnos-
perms. Briefly, in a large number of cases, the primitive
pollen, or prepollen, appears to have germinated in the
old spore fashion via the trilete or monolete suture
 STEEVES 3553

(Taylor and Millay 1979; Taylor 1982). It must be ontogenetic study (Rothwell1971) of the Late Carbonif-
presumed that the sperm which were released within the erous seed fern ovule Callospermarion does indicate a
ovule were motile and propelled themselves to the site ofsubstantial similarity to the pattern found in living
the female gamete in an archegonium (Stewart 1951). gymnosperms.
This is not difficult to visualize since it occurs in the The gymnosperm female gametophyte is consistently
so-called zooidogamous living gymnosperms, the cyc- a large, nutrient-filled structure which develops within
ads and Ginkgo. However, these modem anachronisms the wall of an unshed megaspore. The megaspore
have a pollen tube and it arises from the distal side of the
enlarges substantially, becomes highly vacuolate, and
grain. The pollen tube in these cases does not serve to undergoes a prolonged phase of free nuclear division
deliver the sperm to the egg as in the conifers and the before any partitioning begins. In Ginkgo it is reported
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angiosperms. Rather it is a haustorial device which is that some 8000 nuclei may be formed before partitioning
believed to draw nutrients from the tissue of the occurs and even in pines the number is said to be near
nucellus. The large, motile sperm are released from the 2000 (Foster and Gifford 1974). Subsequently one to
other end of the male gametophyte in a small droplet of many archegonia develop at the apical or micropylar end
fluid and are self-propelled to the archegonium. Only in of the gametophyte. The initial pattern of free nuclear
higher forms, where the sperm are without motility, development has been linked by some workers to the
does the pollen tube grow to the site of the egg and fact that a large volume must be subdivided in the first
deliver the sperm. In conifers it actually forces its wayinstance; but why is the volume large before division
between the neck cells of the archegonium (Foster and begins? This may be an evolutionary heritage relating
Gifford 1974) and in some cases must first penetrate a back to an ancestral form in which a large, food-filled
megaspore wall (albeit not a very thick one) to gain megaspore was discharged to develop independently.
access to the female gametophyte (Chamberlain 1935). The original gymnosperms appear to have departed
There is good reason to-believe that the primitive very little functionally from their free-sporing ancestors,
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prepollen of the seed ferns and cordaites, which germi- at least if we may judge from the living but archaic
nated proximally, produced no pollen tube; that struc- cycads and Ginkgo. These forms in effect package the
ture is, in all cases known, a product of distal germina-materials which will ultimately support the development
tion. Considerable interest is therefore attached to the of the next generation embryo in-the female gameto-
report of the oldest known pollen tube from the middle phyte before the process of embryo development begins
art of the Late Carboniferous Period (Rothwell 1972). (Favre-Ducharte 1958). This phenomenon is seen very
In that report a germinated pollen grain was described inclearly in Ginkgo, in which fertilization frequently does
the pollen chamber of an ovule of the seed fern not occur in a pollinated ovule until after it has been
Callisrophyron. The pollen tube emerged from the distal shed, that is, on the ground (Eames 1955). In such cases
side of the grain and, as in some modem gymnosperms, any possible contribution of the parent sporophyte to the
was a branched structure. One is inclined to suspect thatnext generation sporophyte must be "prepackaged in
its function was haustorial, but the possible early the female gametophyte. In fact Ginkgo is variable in
occurrence of siphonogamy cannot be ruled out. this regard even on the same tree and seeds are also shed
with embryos in various stages of development. In the
The gymnosperm seed modem conifers the situation is somewhat different in
Among the seed plants, the name gymnosperm is that female garnetophyte development and the deposi-
commonly applied to all those in which pollen is tion of nutrient reserves continue after fertilization and
transferred directly to the ovule, within which the male while the embryo is developing so that the reserves are
gametophyte completes its development. Comparative not entirely prepackaged (Favre-Ducharte 1958; Singh
studies of living gymnosperms, strongly supported by 1978). But even here, as in all gymnosperms, it must be
palaeobotanical evidence, indicate that very early in recognized that there is a substantial investment which,
seed-plant history two major evolutionary lines diverged if fertilization does not occur, serves no useful function.
from the progymnosperms, and indeed may even have Whatever its stage of development, if fertilization has
been evident within that ancestral group (Beck 1976a; not occurred, the embryo of Ginkgo appears to continue
Stewart 1981). These are the cycadophyte and the its growth and to germinate in a continuous process,
coniferophyte lines, which have been distinct for ap- environmental conditions permitting. A similar kind of
proximately 350 million years. Nevertheless, through- continuous development culminating in germination has
out the gymnosperms there is a common basic pattern of also been reported for many cycads (Chamberlain
development and structure of the female or megagamet- 1935), but it not possible to generalize. Our common
ophyte. This statement is subject to the limitation that view of a seed with a fully developed or mature embryo
there is not a great deal of developmental information in a state of arrested development does not apply here.
about diverse Palaeozoic ovules, although Rothwell's That this kind of development was probably characteris-
 3554 CAN. J. BOT. VOL. 61, 1983
tic of the Palaeozoic seed plants, seed ferns and
cordaites, is suggested by the fact that, although
detached seeds are common fossils, they very rarely
contain an embryo (Miller and Brown 1973). This is in
sharp contrast with the relative frequency of embryos in
Mesozoic cycad and conifer seeds (Taylor and Millay
1979;Taylor 1982). Upon reflection this may not be too
surprising. If seeds were shed before embryo develop-
ment had begun, those which had not been pollinated
might remain to be preserved. Those containing viable
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pollen would be expected to undergo fertilization and
the completion of embryo development to germination.
Hence there would be no development of a seed bank
which might have resulted in the preservation of
embryo-containing seeds. The retention of the seed until
the embryo has reached a relatively complete stage of
development is characteristic of the modern conifers and
may have been the situation in Mesozoic plants in which
seeds with embryos are more commonly found. One can
visualize the development of a pattern in which seeds are
released with a relatively advanced embryo in a state of
arrested activity as a response to what may have been
seasonably unfavorable climates.
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If one compares the patterns of embryological devel-
opment found in the various groups of gymnosperms
with those of the lower vascular plants, some interesting
contrasts emerge. In the lower groups, such as the ferns,
the pattern of zygote segmentation and subsequent
division is highly regular, perhaps less so than is often
reported but regular none the less. A remarkable feature
of the gymnosperms is their complete departure from
this kind of restricted development. In a pattern which is
unique, the early development of the proembryo is free
nuclear, the number of nuclei which precede segmenta-
tion ranging from 4 in Pinus to more than 1000 in some
cycads. The eggs and zygotes of gymnosperms are
enormous and this division mechanism has been attrib-
uted to the difficulty of segmenting such a large mass of
cytoplasm (Chamberlain 1935). Subsequent develop-
ment of the cellular embryo is also cumbersome by
lower-plant or angiosperm standards. A further remark-
able feature is the extensive occurrence of polyem-
bryony, resulting from both the fertilization of more
than one egg and the cleavage of the products of
individual zygotes. This certainly seems to be inef-
ficient, although it must be acknowledged that it does
constitute a pregerminal selection process since ordinar-
ily only one embryo survives (Berlyn 1962). Finally
there is usually an exuberant development of suspensors
which force the embryos down into the nutritive tissue of
the gametophyte. In Ceratozamia, Chamberlain (1935)
reports suspensors which, when stretched out, reach a
length of 7 to 8 cm. In short, gymnosperm embryogeny
gives the impression of extravagant inefficiency,
although the extant conifers have undergone some
moderation of this extravagance. Sequoia, for example,
seems to have eliminated the free-nuclear ~ h a s from
e its
embryogeny, as has Gnetum among the Gnetopsida.
One would like to know more about the embryos of
Palaeozoic seed plants to gain a better understanding of
this story. New discoveries may provide some answers,
but as already noted, the prospect is discouraging. It
may be suggested that the prior development of a large
and nutrient-filled female gametophyte permits the
embryo sporophyte to begin its development without
nutritional restrictions. This is in sharp contrast with
many of the lower plants, in which the embryo probably
begins its development under rather limiting circum-
stances. However, explaining that a phenomenon is
possible does not give an interpretation of why it
occurred. Even though wasteful, the gymnosperm seed
mechanism may have offered sufficient advantage over
the cryptogams to permit successful competition. It is
possible that this pattern became a kind ofevolutionary
dead end which only drastic revision could remedy.
Finally a word about the fossil history of the gymnos-
permous seed plants. It has been shown that the true seed
plants emerged before the end of the Devonian Period
and expanded rapidly in the subsequent Carboniferous.
A general survey of Coal Age floras, however, indicates
that they were dominated by cryptogams, notably those
of lycopod affinity. Only locally and for limited time
periods did seed plants become a dominant element in
the vegetation (Phillips et al. 1974; Phillips 1981). If the
seed habit offers such advantages for terrestrial sexual
reproduction, why did the seed plants not quickly
replace their more archaic competitors? The answer may
be that the environment of the coal swamps probably
was not truly terrestrial in the "dry l a n d sense of the
word, at least not in those areas where most of the coal
(and fossils) were formed. In the wet environment of a
swamp, free-swimming sperm may have had no great
difficulty in performing their biological role. Thus the
seed plants were successful but not overwhelmingly so.
With the advent of the Permian, and certainly in the
subsequent Mesozoic Era, all this changed and the
cryptogams declined with the swamps that supported
them. Seed plants became dominant and have remained
so ever since except in very special circumstances. It is
interesting to note the parallel in this record with that of
the reptiles, which appeared in the Carboniferous Period
but did not displace the amphibians until the Permian
and Mesozoic inspite of their superior terrestrial repro-
ductive habits. It is also clear that there was a substantial
change in the seed plants themselves as the cordaites
gaveplace to more modern conifers and the seed ferns
were largely (but not entirely) replaced by cycads and
cycadeoids. Although we do not know as much about
the actual seeds of these more modern forms as we
would like, it is probable that the conditions favoring the
 STEE
triumph of the seed habit also led to a streamlining of
some of the more cumbersome aspects of Palaeozoic
seed biology.
Angiosperm seeds
We come now to the seed plants which, from the point
of view of present-day vegetation as well as of this
symposium, are the main focus of interest, the angio-
sperms. As is well known to all botanists, the angio-
sperms make their debut in the fossil record rather
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abruptly in sediments of the latter part of the Early
Cretaceous Period. As new discoveries fill gaps in our
knowledge, the appearance of abruptness is becoming
somewhat tempered, yet there is no strong evidence to
suggest that the flowering plants as such are much older
than the fossil record indicates (Beck 1976b). The seed
ferns were an important plant group in the Carboniferous
Period and greatly diminished in the Permian and
succeeding Mesozoic; yet they did not become extinct
and several specialized groups were present in the
Triassic and Jurassic. It is among these persistent seed
ferns that many palaeobotanists are increasingly search-
ing for angiosperm origins (Dilcher 1979).
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It is beyond the scope of this paper to review current
theories as to how the angiosperm carpel, stamen, and
flower as a whole might have been derived from known
seed-fern fructifications. It is sufficient to say that a
number of quite plausible theories are currently being
debated. It is important also to note that the answer is not
yet at hand. One point, however, is worth commenting
bpon. It has long been a cherished concept that the origin
of the angiosperms, the evolution of the supposedly
primitive bisexual flower, and the rapid expansion and
adaptive radiation of the angiosperms are intimately
related to the phenomenon of insect pollination. That
entomophily has been an important factor in the evolu-
tion both of flowering plants and of certain insect groups
seems to be beyond reasonable doubt (Crepet 1979).
However, the primary role of this phenomenon in the
emergence of angiospermy is now being questioned.
There are two lines of evidence which lead to this doubt.
Contrary to the long-held view that gymnosperms are
all or nearly all wind-pollinated, evidence is emerging
that insects to varying degrees have been pollen vectors
for gymnospermous groups (Dilcher 1979; Taylor 1978;
Taylor and Millay 1979). It has been demonstrated that
se"era1 ~ a l a e o z ~ seed
i c ferns produced pollen grains
which had a diameter many times greater than that
considered maximal for effective wind dispersal. Insect
coprolites containing pollen have been discovered
(Taylor 1982) and evidence of insect chewing in cones
of Cycadeoidea is reported (Delevoryas 1968; Crepet
1972, 1974). While such evidence is not conclusive, it is
becoming increasingly probable that insect pollination
had been around for a long time before the angiosperms
evolved and it seems less reasonable than it once did to
suppose that it was the major stimulus in the emergence
of this group. This conslusion has been advanced and
defended by Meeuse in a number of publications during
the past decade (Meeuse 1979).
As knowledge of the earliest angiosperm reproductive
structures grows, it is becoming clear that unisexual
flowers which give every indication of wind pollination
are just as old as any which are insect pollinated (Dilcher
1979). Both patterns seem to have been present from as
close to the beginning as the record goes. Quite possibly
many of our wind-pollinated forms today, contrary to
widespread belief, have no history of insect pollination
in their ancestry, although others clearly do (Dilcher
1979). If there is a fundamental characteristic which
underlies the early explosive evolution of all angio-
sperms, it does not appear to be entomophily.
The enclosing of the ovules in carpels is of course the
feature from which the angiosperms take their name.
This process could have provided protection against
both unfavorable climatic conditions and herbivores and
thus allowed the ovules themselves to be less elaborately
structured and capable of more rapid development. The
tendency to provide some sort of protection for the
ovules was widespread in the seed ferns with their
cupules, and in fact in some Mesozoic pteridosperms
(such as Caytonia) the ovules were completely envel-
oped, although pollen was apparently carried directly to
the micropyles (Reymanowna 1973). This could have
been an important factor in early angiosperm success,
particularly when the elaboration of a stigmatic surface
began to enhance both pollen catching and microgamet-
ophyte development in wind-pollinated as well as
insect-pollinated flowers. It could also have provided an
effective screening device for eliminating inappropriate
There is, however, another feature, related directly to
the seed itself, which may well be of prime importance.
In 1898 Nawaschin made the remarkable discovery,
soon confirmed by others and recognized as a general
angiosperm characteristic, that the second male nucleus
also effects a fertilization (Maheshwari 1950). Double
fertilization, which results in the development of the
endosperm contemporaneously with the embryo, is not
only a general phenomenon in angiosperms, it is a
unique characteristic. In fact the occurrence of this mode
of fertilization, the origin of which is and probably will
remain unknown because fossils do not preserve this
kind of detail, stands as compelling testimony to the
monophyletic origin of the angiosperms.
There has long been and continues to be debate about
the morphological nature of the endosperm (Mahesh-
wari 1950; Eames 1961). To some, because it results
from a fertilization, it appears to be a second embryo,
the result of a kind of abnormal polyembryony. By
 3556 CAN. J. BOT. VOL. 61, 1983
others, it is regarded as a delayed female gametophyte
programmed to await a fertilization stimulus. Its func-
tional role and its common free-nuclear initial ~ h a s eare
cited in support of this second interpretation. Increas-
ingly, however, botanists have tended to consider such
speculations futile and to look upon the endosperm as a
new departure, based indeed upon the female gameto-
phyte and to some extent replacing it functionally, but
representing an innovative development in vascular-
reproductive biology.
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Although the origin is unknown, the biological
significance of double fertilization is not difficult to
deduce. Indeed several different advantages have been
suggested and it may be that a combinatkn of benefits
led to the adaptive significance of endosperm develop-
ment. In the first place the typically triploid endosperm
should be much more effective in RNA transcription
than a haploid gametophyte because more template sites
are available for the process. In this connection it is
worth noting the participation of two polar nuclei in the
fusion so that triploidy results, rather than just one as
might have been expected. Also recall that the ploidy
level is even higher in some cases, for example five ploid
For personal use only.
in the familiar lily or Fritillaria type and nine ploid in
the Peperomia type. The higher ploidy levels may
indeed confer some metabolic efficiency upon the tissue
which provides the embryo support system. A further
advantage might arise from the incorporation of a male
genome into this support system either because of some
sort of resulting heterosis or in terms of an enhanced
compatibility between embryo and nurse tissue.
One of the chief advantages of double fertilization is
seen in terms of energy efficiency. The development in
advance of fertilization of a large female gametophyte,
the role of which is to support the embryo, is wasted
effort if fertilization does not occur. It is, therefore,
argued that the coupling of this development to the
fertilization process eliminates this potential waste.
Only when pollination and fertilization have been
achieved does the nutrient-rich storage depot develop.
Considering the hazards of the pollination process this
may well be a significant consideration.
There is, however, a further consideration relating to
the reproductive cycle in angiosperms which may have
had more to do with the actual origin and early radiation
of the group. This discussion draws heavily upon
concepts developed by Stebbins, who has given consid-
erable thought to the question of angiosperm origins
(Stebbins 1974). His theory has a number of aspects, but
reference is made here only to those which involve the
seed. Stebbins, in agreement with many palaeobotan-
ists, believes that the angiosperms did not come into
existence very long before-theymade their appearance in
the fossil record. Hence, he argues that they evolved
very rapidly. Rapid evolution is most probable in an
environment which applies strong selective pressures
and Stebbins suggests that, in the tropical or warm
temperate climate of angiosperm origin, seasonal varia-
tion of a wet and dry type may have been a major
influence. These conditions could result in a relatively
brief period during which sexual reproduction, or indeed
any development at all, could be accomplished and
might be expected to place a premium upon the rapid
completion of the process with the production of viable
seeds. More recently Retallack and Dilcher (198 1) have
suggested that a marine coastal environment was more
likely to have been the scene of these events. In the
preangiosperms the pressure for accelerated develop-
ment led, Stebbins argues, to modifications of both male
and female gametophytes. Quick germination of the
pollen grain and rapid growth of the pollen tube,
enhanced by the development of special receptive and
transmitting tissues in the carpel, occurred on the male
side. At the same time, the development of the female
gametophyte, prior to fertilization, was drastically
reduced to the well-known seven-celled, eight-nucleate
embryo sac which is the basic angiosperm type. If
fertilization occurred, the necessary embryo support
system was then rapidly developed along with the
embryo. The cytological condition of the endosperm, as
has been pointed out, is believed to favor both its rapid
development and its efficiency as a metabolically active
tissue. Thus a very quick and efficient reproductive
system replaced the more cumbersome ancestral gym-
nospermous system. This is an attractive interpretation
of the unique features of angiosperm seed development.
It is not, however, to be considered as the only
phenomenon which contributed to angiosperm success.
In the context of accelerated development, Stebbins
has called attention to the angiosperm embryo which
differs strikingly from that of almost all living gymno-
sperms. It has been pointed out earlier that in all extant
gymnosperms with the exception of Sequoia and Gne-
tum the initial phase of embryo development is one of
free nuclear division, with wall formation coming later
and often remaining incomplete. In the angiosperms, by
contrast, wall formation follows immediately upon
mitosis and the early segmentation of the embryo is
highly regular. Indeed it is so regular that a classification
of types has been devised, although admittedly recent
work suggests that more variations occur than had been
appreciated. Stebbins argues that this more direct
embryo development accelerates the process of seed
maturation and represents a significant evolutionary
departure from the ancestral gymnosperm pattern. There
have been occasional reports of an early free-nuclear
phase in the embryos of particular angiosperms, for
example in the genus Paeonia (Yakovlev and Yoffe
1957; Cave et al. 1961); but this is at most an
exceptional phenomenon and it has been challenged
 STEEVES
(Murgai 1959). It is worth recalling that in the conifers,
the only gymnosperms which have persisted on a large
scale, there is a clear tendency to reduce the extent of
free-nuclear development of the proembryo prior to wall
formation. In Sequoia it has been eliminated complete-
ly. Possibly the advantages of more direct segmenta-
tion have been important here too.
The pattern of direct segmentation in angiosperms,
although different in detail, is not very unlike that which
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is found in all extant lower vascular plants (and
bryoph)tes and algae as well). In one sense it would
seem that the angiosperms have returned to the tradi-
tional approach to embryogeny from which the more
ancient seed plants represent an aberrant but rather
massive departure. Unfortunately, as has been pointed
out, we know nothing about the embryology of the
ancestral seed plants. The angiosperms could conceiva-
bly have arisen from a gymnosperm line which never
adopted a free-nuclear embryonic phase. However, the
occurrence of this stage in such widely separated
modem gymnosperms as the conifers, the cycads,
Ginkgo, and Ephedra argues for its ancestral universal-
ity. A return to more traditional embryogeny could then,
For personal use only.
as Stebbins suggests, have constituted a significant
evolutionary step in favor of reproductive efficiency.
This line of thought leads to some additional consider-
ations. A survey of the life cycles of the lower vascular
plants with free-living gametophytes dependent upon
their own resources for the early nurture of the new
sporophyte generation suggests that the embryo is rarely
if ever provided with any superabundance of nutrient
reserves. Direct and efficient embryo development
leading quickly to independence appears to be a neces-
sary condition for survival. The advent of the seed habit,
the retained megaspore and female gametophyte with
abundant nutrients derived from the parent sporophyte,
could very well have removed the traditional nutritional
restraints from the developing embryo. Under these
circumstances the large egg, which after fertilization
could not easily be partitioned, may have been possible.
So also the development of multiple embryos may have
been an acceptable device to provide insurance that at
least one would survive and possibly to permit a certain
degree of internal selection for vigour. These seemingly
wasteful processes may have had no significant deleteri-
ous effects for the early seed plants, allowing them to be
selected for whatever small advantages they could have
provided. Thus a pattern was established which has
persisted in several lines of extant gymnosperms.
Although we do not know, and probably never can
know, how the change occurred, clearly the emergence
of the angiosperms was accompanied by far-reaching
alterations in the status of the early embryo. The delay in
the development of the endosperm until after fertiliza-
tion eliminated the ready-made support system charac-
3557
teristic of gymnosperms. The restricted and highly
regular division pattern of early embryogeny seems to
accelerate the completion of seed development. It is also
possible that this pattern is necessitated by a limitation of
resources available to support embryo development at
least in the early stages. Embryologists of a few decades
ago, seeking principles of early embryo development in
angiosperms, devised one often called the Law of
Parsimony. In essence this law states that the zygote in
its segmentation undergoes the minimum number of
divisions necessary to produce the required structures,
"No more cells are produced by the embryo than are
absolutely necessary" (Johansen 1950). It may be
reasonable to consider the Dossibilitv that there is a
physiological parsimony in terms of nutrients which
underlies the morphological expression of that prin-
ci~le.
With so many species of angiosperms extant today,
there are many patterns of development of embryo and
endosperm and one cannot make entirely consistent
generalizations. Nevertheless there are several lines of
evidence which suggest that in most cases, although the
endosperm is at hand to support the later and very rapid
stages of embryo development, in the critical early
stages the embryo must find other sources. In some cases
endosperm development is very rapid and embryo
development is delayed, but the fact remains that in most
cases endosperm is simply not present except in rudi-
mentary form in the critical early stages of embryogeny
(Brink and Cooper 1947; Raghaven 1976). Even when
present, it does not seem to be drawn upon until the late
globular or early heart stage. The embryo of Iceland
poppy recently studied by Olson (198 1) shows this very
clearly. Digestion of the endosperm does not appear to
occur before the late globular stage 9 or 10 days after
pollination. Early embryo development thus appears to
be sustained by nutrients available in the embryo sac,
possibly supplemented by additions from the persistent
synergid and other sources. This conclusion is supported
by reports that when seed development fails in certain
types of incompatibility in which the endosperm devel-
ops incompletely or abnormally, the early phases of
embryogeny are not much affected and it is the later
stages which are arrested (Brink and Cooper 1947).
A further line of evidence is found in the structure of
the embryo itself. A structure known as a suspensor is a
common feature of the embryos of many groups of
vascular plants, but in the angiosperms it appears that
this embryonic organ takes on special functions (Steeves
and Sussex 1972'1. In a number of cases which have been
investigated in detail there is a rapid differentiation of
the suspensor and its cells develop in such a way that
they appear to be highly active metabolically and are
often provided with typical transfer cell wall structure
(Schulz and Jensen 1969; Newcomb and Fowke 1974;
 3558 CAN. 1. BOT. VOL. 61, 1983

Yeung and Clutter 1978). Moreover, there is evidence Conclusions

both cytological and physiological that the metabolic Since this commentary has wandered freely and rather
activity of the suspensor is different from that of the speculatively through diverse plant groups, past and
organogenetic part of the embryo (Sussex et al. 1973). It present, and has touched upon a range of topics, it is
looks as though, in many cases, the so-called suspensor, appropriate to summarize the salient points.
rather than merely orienting the embryo or forcing it into In comparing modem angiosperm seeds with the
the nutrient tissue, serves as an absorbing organ for the freely shed spores of the original vascular plants, one
embryo and probably also synthesizes specific metabol- cannot fail to be impressed by the scope of the
ites for the embryo proper from the basic materials evolutionary change which has occurred. The ancient
absorbed. The significance of this role of the suspensor structure of the resistant land spore has been retained in
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has been demonstrated experimentally by Yeung and the pollen grain, but its function has been adapted from
Sussex (1979) in a study in which the growth in vitro of dispersal to that of terrestrial gamete transfer. The male
isolated young embryos of Phaseolus coccineus was gametophyte has been transformed into an agent which
shown to be enhanced by the presence of the suspensor. precisely delivers the sperm to the egg. Meanwhile the
It is an intriguing correlation that the suspensor differen- female gametophyte has been reduced to little more than
tiates very early and often begins to senesce at about the a pro forma existence and its embryo support role
time that the embryo proper gives evidence of beginning assumed by a new and efficient nurse tissue, the
to draw directly upon the endosperm. endosperm. In the end the embryo has become increas-
Another intriguing aspect of this question is the ingly equipped to draw directly upon the parent sporo-
evidence that in many cases the endosperm is in part at phyte.
least bypassed in favor of direct dependence of the Reviewing this series of achievements, one is tempted
embryo upon the resources of the parent sporophyte. to speculate on the future trends of seed evolution.
Such features as the development of perisperm, nucellar Given the wide diversity of seeds which even a cursory
For personal use only.

in origin, which partially or even completely replaces survey of the modern seed plants reveals, it is highly
the endosperm, are well known and not uncommon. probable that potentially significant innovations are
Even more striking is the evidence that the suspensor even now being tested and refined in the crucible of
draws directly upon parental sporophyte tissues. Often natural selection. The contributions which follow in this
at the micropylar end of the embryo sac it extends well symposium may thus be expected to provide some
into the surrounding nucellar and integumentary tissues. insight into the future direction of an evolutionary
Moreover there are numerous instances in which sus- process which began 350 million years ago but has
pensors develop elaborate haustorial extensions which, certainly not yet run its full course.
although sometimes confined to the embryo sac and
developing endosperm, in other instances extensively
penetrate parental sporophyte tissues (Maheshwari Acknowledgements
1950). It would appear, therefore, that in some angio- It is a pleasure to acknowledge the contribution which
sperms, and perhaps in many, there is a tendency to shift Drs. J. F. Basinger, G. P. Berlyn, A. R. Olson, and I.
the dependency of the early embryo directly to the parent M. Sussex have made to this paper by their helpful
sporophyte and away from an intermediate gametophyte criticisms and suggestions.
generation or some modified form of that generation.
Perhaps this intermediary, which is a legacy of the
ANDREWS, H. N. 1963. Early seed plants. Science (Washing-
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