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Comparative embryology of basal angiosperms
William E Friedman
Recent phylogenetic analyses of basal angiosperms have
identified those lineages central to the study of the origin and
early diversification of flowering plants. As we begin to
understand the early evolution of endosperm developmental
patterns in flowering plants, it is apparent that we know little
about the other basic embryological features of basal
angiosperms, such as the nature of the female gametophyte
and even whether a process of double fertilization occurs.
that little work remains to be done on the documentation
and discovery of developmental patterns associated with
the fertilization process, embryos, and endosperms. Yet, for
all of the recent progress in analyzing the phylogenetic
relationships of plants and deciphering molecular developmental programs in model systems, much of the
organismic diversity of extant plants has yet to be studied,
even at the most rudimentary level.
Addresses
Department of Environmental, Population and Organismic Biology,
University of Colorado, Boulder, Colorado 80309, USA;
e-mail: [email protected]
This review focuses on our current understanding of the
comparative embryology of basal angiosperms and examines the impact of recent advances in phylogenetic
systematics on the area of early flowering plant evolution.
In addition, the import of recent proposals to move beyond
century-old typological schemes to a more evolutionary
and developmental framework for the description of
embryological process will be discussed.
Current Opinion in Plant Biology 2001, 4:14–20
1369-5266/01/$ — see front matter
© 2001 Elsevier Science Ltd. All rights reserved.
Introduction
Had Current Opinions in Plant Biology published its fourth
volume in 1901 instead of 2001, the focus of a brief
review/perspective of the previous few years of research in
the area of comparative embryology would have been an
enormous undertaking. Just over a century ago, international competition was keen to discover and document
fertilization processes, and embryo and endosperm developmental patterns in a wide diversity of plants. In Japan in
1896, motile sperm were discovered in seed plants [1,2]. In
Russia (1898) and France (1899), a second fertilization event
(double fertilization) that initiates endosperm in flowering
plants was reported [3,4]. Within months of the discovery of
double fertilization in two species of lily, workers in France,
Germany, Japan, Great Britain, and the United States raced
to determine whether this phenomenon was a general feature of flowering plants and to interpret its evolutionary
significance. The last half of the nineteenth century, as well
as the first decade of the twentieth century was truly the
golden age of comparative biology, a period dominated by
evolutionary and developmental morphologists and
anatomists, whose focus was on organisms and the variation
inherent among plant life cycles.
Of course, volume four of Current Opinions in Plant Biology
will be published in 2001 and this review/perspective on
the field of comparative embryology will necessarily differ
from what might have been written a century ago. We live
in a world in which molecular systematics and molecular
developmental biology are dominant fields within biological research; where the focus has shifted from the organism
and the breadth of organismic diversity to the genome and
the more phylogenetically limited study of a small number
of ‘model systems.’ The inference might be that, more
than 150 years after comparative plant biology emerged as
a major discipline, everything about the basic biology and
variation in reproductive process in plants is known; and
Phylogenetic context for basal angiosperms
The importance of understanding the embryological features
of early angiosperm lineages cannot be overemphasized
because flowering plants are thought to be defined, in many
ways, by their reproductive biology. Angiosperms, unlike all
(or almost all) other groups of extant seed plants, possess a
reduced male gametophyte (of three cells at maturity), a
reduced female gametophyte (of seven cells and eight nuclei
at maturity), a process of double fertilization, endosperm as
an embryo-nourishing tissue, and a cellular pattern of
embryogeny. In order to analyze the origin and early evolution of flowering plants, a clear formulation of the
phylogenetic interrelationships of basal angiosperms is
essential [5••]. With robust phylogenetic hypotheses, evolutionary interpretation of the comparative biological features
of angiosperms can be used to infer and reconstruct the
diversification of plant reproductive patterns.
For over a century, the identification of the earliest lineages of flowering plants was controversial and uncertain.
Beginning in 1999, a series of independent analyses
yielded a remarkable consensus on the most basal
angiosperm lineages. These phylogenetic analyses
[6••,7,8,9••,10•,11,12,13••,14,15•,16••] identify three monophyletic groups that comprise a basal (i.e. paraphyletic)
grade of angiosperms: Amborella trichopoda, Nymphaeales
(Nymphaeaceae plus Cabombaceae), and a clade that
includes Illiciaceae, Trimeniaceae, Schisandraceae and
Austrobaileyaceae. It is currently unclear whether
Amborella, Nymphaeales, or Amborella plus Nymphaeales is
the sister group to all other angiosperms (Figure 1).
There have been additional recent phylogenetic findings
about the major relationships among angiosperms.
Although the term ‘dicots’ still (unfortunately) appears in
the literature, flowering plants with two cotyledons in the
Comparative embryology of basal angiosperms Friedman
15
Figure 1
(a)
Amborellaceae
(b)
Nymphaeaceae
(c)
Cabombaceae
Nymphaeaceae
Cabombaceae
Nymphaeaceae
Cabombaceae
Amborellaceae
Amborellaceae
Illiciaceae
Illiciaceae
Illiciaceae
Schisandraceae
Schisandraceae
Schisandraceae
Trimeniaceae
Trimeniaceae
Trimeniaceae
Austrobaileyaceae
Austrobaileyaceae
Austrobaileyaceae
All other angiosperms
including eumagnoliids,
eudicots and monocots
All other angiosperms
including eumagnoliids,
eudicots and monocots
All other angiosperms
including eumagnoliids,
eudicots and monocots
Current Opinion in Plant Biology
Hypothesized relationships of basal angiosperms. Recent phylogenetic
analyses indicate that (a) Amborellaceae (Amborella trichopoda),
(b) Nymphaeales (Nymphaeaceae plus Cabombaceae), or
(c) Amborellaceae plus Nymphaeales is sister to all other angiosperms.
All recent phylogenetic analyses conclude that Amborella trichopoda,
Nymphaeales and a clade that includes the Illiciaceae,
Schisandraceae, Trimeniaceae and Austrobaileyaceae comprise a
grade of flowering plants that are basal.
embryo clearly comprise a paraphyletic group that is no
longer recognized by evolutionary biologists. Most (i.e.
95% of) dicotyledonous flowering plants, however, belong
to a major monophyletic group [17], the eudicots (which
are identified by the synapomorphy of tricolpate pollen).
Another group, the eumagnoliids (comprising the
Laurales, Magnoliales, Winterales, and Piperales), may
constitute an additional monophyletic lineage of dicotyledonous flowering plants (this finding is currently weakly
supported). Phylogenetic analyses of flowering plants continue to demonstrate that monocots are a robust monophyletic group. Currently, the relationships of monocots,
eudicots and eumagnoliids are uncertain (Figure 2).
there is little evidence (one way or the other) that double
fertilization occurs in any of the most basal angiosperm lineages [5••,20••]. All basal angiosperms are known to produce
an endosperm, but the question of its developmental origin
remains unresolved. It is entirely possible that endosperm in
Amborella and other basal angiosperms is developmentally
derived from the central cell of the female gametophyte
alone, and as such, is a genetically maternal tissue [20••].
Alternatively, a second fertilization event within the central
cell of the female gametophyte, as has been definitively
documented in derived monocots and eudicots, might initiate the formation of endosperm in Amborella. Only careful
investigations of female gametophyte development and the
fertilization process in the most basal angiosperms will
reveal the developmental origin of endosperm in these taxa.
The female gametophyte and double
fertilization in basal angiosperms
For the first time, we know which groups of plants are central to reconstructing the evolution of patterns of
embryology among early angiosperms. The question is,
what do we actually know about the nature of embryological
features in basal angiosperms?
Although Amborella may be the sister group to all other
extant angiosperms and, as such, central to the determination of plesiomorphic character states for flowering plants,
almost nothing is known of its embryology (see also
Update). Embryo and endosperm development of Amborella
are entirely unknown. Even the question of whether double
fertilization occurs in Amborella has never been examined.
Surprisingly, a century after it was ‘concluded’ that double
fertilization is a defining feature of all angiosperms (except
where it has been lost, as in the Podostemaceae [18,19]),
The assumption, now more than a century old, that a
seven-celled, eight-nucleate, female gametophyte is a
defining feature of flowering plants, which evolved in their
common ancestor, may also prove premature. The only
recent work on female gametophyte development in the
most basal angiosperm lineages involves members of the
Nymphaeaceae and Cabombaceae [21–23]. Interestingly,
these papers report that the mature female gametophyte in
Nymphaea and Cabomba has four nuclei and four cells at
maturity: one polar nucleus in a central cell, one egg cell,
and two synergids. These findings contradict earlier studies that detected a more typical seven-celled,
eight-nucleate female gametophyte in Nymphaeales
[24–29]. It is possible that natural variation in female
gametophyte structure exists in basal angiosperms, or that
some of these studies are incorrect.
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Growth and development
Figure 2
Amborellaceae
Cabombaceae
Nymphaeaceae
Illiciaceae
Schisandraceae
Trimeniaceae
Austrobaileyaceae
Ceratophyllum
Monocots
Winterales
Laurales
Eumagnoliids
Piperales
Magnoliales
Chloranthaceae
Current Opinion in Plant Biology
Eudicots
Major monophyletic groups of angiosperms. Although recent
phylogenetic analyses have identified the earliest divergent lineages of
extant angiosperms, there is much uncertainty about the phylogenetic
relationships of other relatively basal angiosperm lineages. For example,
the phylogenetic placement of monocots and eudicots is poorly resolved
at present. The positions of Chloranthaceae and Ceratophyllum remain
ambiguous and are highly variable between analyses. There is currently
weak support for the monophyly of eumagnoliids, which include
Piperales, Winterales, Laurales and Magnoliales.
If members of the Nymphaeales do indeed produce a fourcelled female gametophyte, and if Nymphaeales should be
resolved as sister to all other angiosperms, then a fourcelled, four-nucleate female gametophyte could be
plesiomorphic for flowering plants. The implications of
such a finding would be that a seven-celled, eight-nucleate
female gametophyte might be derived (apomorphic)
among angiosperms. Moreover, endosperm might be
diploid in its plesiomorphic state (assuming that it actually
arises from a second fertilization event [see above]) or even
haploid, if it could be shown that no second fertilization
event occurred! Although these evolutionary developmental
scenarios may appear to be highly speculative, the fact is that
we currently lack sufficient information about the reproductive biology of basal angiosperms to be confident about what
constitutes a plesiomorphic condition and whether certain
characters, long believed to be synapomorphies of flowering
plants, are indeed so.
Endosperm development and evolution in
basal angiosperms
Recently, there has been a concerted effort to study the
developmental patterns expressed by endosperms in basal
angiosperms [30••,31••]. The goals of these studies have
been twofold: to determine the plesiomorphic pattern of
endosperm development in flowering plants and to examine the evolutionary diversification of endosperm
development among early divergent lineages. Flowering
plant endosperm has long been characterized into three
basic developmental patterns: free nuclear, (ab initio) cellular, and helobial. Free nuclear endosperm development
always begins with a syncytial phase (i.e. mitosis without
cytokinesis), which is usually followed by a process of cellularization (i.e. cytokinesis without mitosis) and
additional cellular growth (i.e. mitosis coupled with cytokinesis). Cellular endosperm development is characterized
by the coupling of cytokinesis with mitosis from the very
first division of the endosperm. In helobial endosperm, the
first division of the primary endosperm nucleus is immediately followed by a cell division to yield a two-celled
endosperm. Syncytial development then occurs in one or
both of these cellular compartments (and may later be
followed by a process of cellularization).
Although free nuclear endosperm has long been known to
be the most common ‘type’ among flowering plants, this
pattern of endosperm development does not occur among
the most basal angiosperms. Rather, cellular patterns of
endosperm development are prevalent among basal
angiosperms and parsimonious character optimization onto
the most recent angiosperm phylogenies indicates that cellular endosperm development is likely to be plesiomorphic
among flowering plants [31••].
It is clear that both helobial and free nuclear endosperms
have originated many times over the course of flowering
plant evolution [31••]. It is unclear whether cellular
endosperm development has ever evolved from a free
nuclear or helobial pattern. Interestingly, helobial
endosperm development, a pattern common among monocots, also evolved within the Nymphaeales in the common
ancestor of the Cabombaceae [31••].
Although free nuclear endosperm is not present in any of
the most basal angiosperms, free nuclear development is
found in several basal monocots [32] (however, most of
these reports are extremely old and could be erroneous
descriptions of helobial development), eudicots [30••] and
some members of the eumagnoliids (specifically, derived
Lauraceae [33]). Free nuclear endosperms of basal eudicots have recently been studied in Platanus [30••], Papaver
[34,35] and Ranunculus [36–38]. When analyzed within a
phylogenetic context, free nuclear endosperm development has likely evolved at least four separate times within
the eudicots [30••], perhaps several times within the
monocots, and once within the Lauraceae [33]. An important point is that the free nuclear endosperms of model
system taxa such as Arabidopsis (a eudicot) and Zea (a
monocot) clearly represent derived developmental patterns among angiosperms; thus they are homoplasious (i.e.
have evolved separately) with respect to each other, as well
as to the free nuclear endosperms of various basal eudicots.
Comparative embryology of basal angiosperms Friedman
Recently, both Olsen et al. [39] and Brown et al. [40] have
called attention to the high degree of overall similarity, at
the cell biological level, of the processes of free nuclear
development and centripetal cellularization in the
endosperms of Arabidopsis and grasses such as Zea.
Moreover, both groups of workers have suggested that
the development of free nuclear endosperms in these
highly derived angiosperms is at least superficially similar to the free nuclear and centripetal cellularization
patterns expressed by the female gametophytes of
nonflowering seed plants.
Clearly, the free nuclear and centripetal cellularization patterns of development found in the endosperms of highly
nested eudicots (e.g. Arabidopsis), basal eudicots (e.g.
Platanus and Ranunculus) and monocots (e.g. Zea), and the
female gametophytes of most nonflowering seed plants
[41] are all strictly homoplasious. Given this important
evolutionary context, it is intriguing to imagine that
ancient developmental programs for syncytial growth and
subsequent cellularization might have been recruited each
time a free nuclear pattern of endosperm evolved from a
cellular (or helobial) ancestral pattern.
Alternatively, specific patterns of cell biological development and gene expression associated with the free nuclear
phase and the process of cellularization in these diverse
syncytial systems might be expected to differ. For example, the developmental origin of anticlinal walls in free
nuclear endosperms has long been controversial [42,43•],
with various workers describing cytoskeleton and cellplate patterns during the initial cellularization of the
syncytial stage that appear to differ among taxa. An evolutionary perspective that has not been explicitly
considered by cell and molecular developmental biologists is that some of the reported pattern-level differences
may be real and indeed reflect the independent evolution
of syncytial endosperm in diverse angiosperm lineages. It
is essential to remember that although the cellular
endosperms of flowering plants may all be homologous (at
the level of developmental pattern), free nuclear
endosperms are not, from an evolutionary perspective, all
one ‘thing’ (the same is true of helobial endosperms). It
would be most useful if future cellular and molecular
studies of free nuclear endosperms explicitly compared
the endosperms of groups that have independently
acquired this pattern of development.
The bipolar nature of endosperm
A recent study of a broad selection of basal angiosperms
reveals an important underlying developmental commonality that is expressed during endosperm development
[31••]. Endosperms of basal angiosperms, whether cellular,
free nuclear, or helobial, are distinctly bipolar and express
independent patterns of development in what have been
termed the ‘chalazal domain’ and the ‘micropylar domain’
[31••]. Even when the entire endosperm is initially free
nuclear, as in Platanus (a basal eudicot), the cytological
17
organization of endosperm in the chalazal domain (which is
densely cytoplasmic with no large vacuoles) has been
reported to be radically different from that in the micropylar domain (where a parietal band of cytoplasm surrounds a
large central vacuole). Moreover, the process of cellularization in each domain in Platanus is temporally separate and
cell biologically distinct. Cell walls are formed simultaneously throughout the chalazal domain, but centripetally in
the micropylar domain [20••].
It is interesting to note that in Arabidopsis, a densely cytoplasmic free nuclear chalazal region forms, and at the time
when the rest of the endosperm cellularizes this chalazal
cytoplasm remains free nuclear [40,43•,44,45,46••]. Other
highly derived free nuclear taxa in which chalazal
endosperm development differs from that of the rest of the
tissue include Zea, Glycine, and Helianthus [47–51]. As might
be expected, differential patterns of gene expression in the
micropylar and chalazal regions in Arabidopsis [45] and Zea
[52–55] have recently been documented. Unfortunately, little, if anything, is known of gene expression in endosperms
of basal angiosperms or any angiosperms with either a
cellular or a helobial pattern of endosperm development.
Among basal angiosperms with helobial endosperms, the
chalazal domain and the micropylar domain are defined by
the first cell division, which yields a two-celled
endosperm. The micropylar domain initiates a free nuclear
pattern of development. The chalazal domain may,
however, undergo free nuclear development, cellular
development, or no further nuclear or cellular proliferation
at all [31••]. Thus, the bipolar nature and independence of
developmental fate between micropylar and chalazal
domains has produced at least three basic patterns among
basal angiosperms with helobial endosperms [31••,56].
Among angiosperms with a cellular pattern of endosperm
development, the chalazal and micropylar domains are not
always defined or tightly correlated with the first cell division. Rather, a chalazal region with limited cell
proliferation and a micropylar region with more extensive
cell proliferation emerge during the early development of
the endosperm [31••].
Clearly, the developmental independence of micropylar
and chalazal domains among basal angiosperms may be
general to all angiosperm endosperms. A most intriguing
aspect of the underlying bipolar nature of endosperm,
whether free nuclear, cellular or helobial, is that this pattern is strongly reminiscent of the morphogenetic
principles that govern the organization of flowering plant
embryos [5••,20••,31••] (principles of embryo development have been recently reviewed [57]). Both embryos
and endosperms (at least plesiomorphic endosperms)
undergo an initial, unequal partitioning of the first cell, and
this is followed by differential patterns of development at
the two poles. Indeed, some of the recently published
[31••] and yet to be published (SK Floyd, personal
18
Growth and development
communication) micrographs of basal angiosperm endosperms are remarkably embryo-like. Kranz et al. [51,58]
have also called attention to the highly embryo-like organization of in-vitro-formed endosperms of Zea, in which
one pole is globular with smaller cells and the other pole is
roughly filamentous with larger cells, much like a suspensor.
The embryo-like nature of endosperms among basal
angiosperms may have important implications for the
analysis of the evolutionary homology of endosperm. For
over a century, a debate has focused on whether
endosperm represents a highly modified supernumerary
embryo or a sexualized modification of a component of
female gametophyte development [20••,59,60]. Although
many basal angiosperm endosperms (and even some
derived angiosperm endosperms, such as in vitro Zea) are
embryo-like, comparative information on the underlying
molecular programs of endosperm and embryos among
basal angiosperms will be critical to the evaluation of these
alternative hypotheses.
One final caveat relating to endosperm development
among basal angiosperms: although many basal
angiosperms have been categorized into one of the three
basic endosperm typologies (i.e. cellular, free nuclear, or
helobial), it is probable that a significant number of these
reports contain serious errors. For example, several
recent studies of endosperm development in basal
angiosperms show that previous reports were incorrect:
Lactoris and Drimys (both magnoliids) were originally
reported to be free nuclear, but are, in fact, cellular
[61,62]; Platanus (a basal eudicot) was originally reported
to be cellular, but is, in fact, free nuclear [30••]; and
Mahonia (a basal eudicot) was reported to be free nuclear,
but is definitely cellular (SK Floyd, WE Friedman,
unpublished data). In many other basal angiosperm taxa,
conflicting reports of endosperm developmental patterns
remain unresolved [30••].
Conclusions
In just the past year alone, more papers have appeared on
the molecular phylogenetics of basal angiosperms than on
the actual biology of basal angiosperms. In the past three
years, more review articles have appeared on the molecular genetics of female gametophytes, embryos and
endosperms of ‘model system’ flowering plants than primary papers on these basic life-cycle components in all of
the basal angiosperms. These comments are not intended
as a slight of the recent advances of molecular systematics
and model system molecular developmental biology. The
remarkable and important advances in these disciplines
have fundamentally recast the nature of inquiry in modern
biology. Rather, as Endress [63] and others have argued
recently, what is needed is a balance between the molecular sciences and the organismic sciences. If we are to
ultimately gain deeper insights into the origin and evolution of flowering plants from both phylogenetic and
molecular developmental perspectives, documentation of
the still largely unknown organismic diversity of structure
and pattern in these critical organisms will be essential.
Update
Recently, research on the embryology of Amborella was
published by Tobe et al. [64]. For the first time, data are
presented that describe diverse reproductive features
including anther anatomy, ovule anatomy and morphology,
female gametophyte development (eight-nucleate, sevencelled) and endosperm development (cellular). No data
were presented that bears on the question of whether a
second fertilization event initiates endosperm in Amborella,
and thus, this remains a question that is open for investigation. Tobe et al. also analyzed embryological character
distribution within basal angiosperms in order to suggest
the nature of plesiomorphic reproductive character states
for angiosperms as a whole.
Acknowledgements
I thank Sandra Floyd for helpful discussions about the evolution of
embryological features of basal angiosperms; Joe Williams and Pam Diggle
for helpful comments for the improvement of the manuscript; and the
National Science Foundation (USA) for support of my research.
References and recommended reading
Papers of particular interest, published within the annual period of review,
have been highlighted as:
• of special interest
•• of outstanding interest
1.
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2.
Ikeno MS: Spermatozoid of Cycas revoluta. Bot Mag Tokyo 1896,
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Nawaschin SG: Resultate einer Revision der
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5.
••
Friedman WE, Floyd SK: The origin of flowering plants and their
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This paper deals explicitly with the character evolution implications of the
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6.
••
Mathews S, Donoghue MJ: The root of angiosperm phylogeny
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One of the first papers to identify Amborella, Nymphaeales and Illiciales as
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A thorough analysis of basal angiosperm phylogeny that was published in a
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•
from multiple genes as a research tool for comparative biology.
Nature 1999, 402:402-404.
One of the first papers to identify Amborella, Nymphaeales and Illiciales as
the most basal grade of angiosperms on the basis of gene sequence.
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•• changes in noncoding chloroplast DNA: interpretation, evolution,
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This phylogenetic analysis finds support for the Nymphaeales as sister to all
other angiosperms on the basis of an indel.
14. Graham SW, Olmstead RG: Utility of 17 chloroplast genes for
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15. Doyle JA, Endress PK: Morphological phylogenetic analysis of
•
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A comparative examination of molecular data and morphological data relating to the phylogenetic relationships of basal angiosperms, and more
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The free nuclear endosperm of Platanus, a basal eudicot, is examined
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31. Floyd SK, Friedman WE: Evolution of endosperm developmental
•• patterns among basal flowering plants. Int J Plant Sci 2000,
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A comparative study of endosperm development in 13 basal angiosperms.
The plesiomorphic features of endosperm development in flowering plants
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