William E. Friedman

The evolution of plant development

The last decade has witnessed a resurgence in the study of the evolution of plant development, combining investigations in systematics, developmental morphology, molecular developmental genetics, and molecular evolution. The integration of phylogenetic studies, structural analyses of fossil and extant taxa, and molecular developmental genetic information allows the formulation of explicit and testable hypotheses for the evolution of morphological characters. These comprehensive approaches provide opportunities to dissect the evolution of major developmental transitions among land plants, including those associated with apical meristems, the origins of the root/shoot dichotomy, diversification of leaves, and origin and subsequent modification of flower structure. The evolution of these major developmental innovations is discussed within both phylogenetic and molecular genetic contexts. We conclude that it is the combination of these approaches that will lead to the greatest understanding of the evolution of plant development.

Identification of diploid endosperm in an early angiosperm lineage

In flowering plants, the developmental and genetic basis for the establishment of an embryo-nourishing tissue differs from all other lineages of seed plants. Among extant nonflowering seed plants (conifers, cycads, Ginkgo, Gnetales), a maternally derived haploid tissue (female gametophyte) is responsible for the acquisition of nutrients from the maternal diploid plant, and the ultimate provisioning of the embryo. In flowering plants, a second fertilization event, contemporaneous with the fusion of sperm and egg to yield a zygote, initiates a genetically biparental and typically triploid embryo-nourishing tissue called endosperm. For over a century, triploid biparental endosperm has been viewed as the ancestral condition in extant flowering plants. Here we report diploid biparental endosperm in Nuphar polysepalum, a basal angiosperm. We show that diploid endosperms are common among early angiosperm lineages and may represent the ancestral condition among flowering plants. If diploid endosperm is plesiomorphic, the triploid endosperms of the vast majority of flowering plants must have evolved from a diploid condition through the developmental modification of the unique fertilization process that initiates endosperm.

The four-celled female gametophyte of Illicium (Illiciaceae; Austrobaileyales): implications for understanding the origin and early evolution of monocots, eumagnoliids,and eudicots

The recent consensus that Amborellaceae, Nymphaeales, and Austrobaileyales form the three earliest-diverging lineages of angiosperms has led comparative biologists to reconsider the origin and early developmental evolution of the angiosperm seven-celled/eight-nucleate (Polygonum-type) female gametophyte. Illicium mexicanum (Illiciaceae; Austrobaileyales) develops a four-celled/four-nucleate female gametophyte. The ontogenetic sequence of the Illicium female gametophyte is consistent with that of all other Austrobaileyales and also with all Nymphaeales and is likely a plesiomorphy of angiosperms. A character analysis based on more than 250 embryological studies indicates that a transition from an ancestrally four-celled/four-nucleate Illicium-like female gametophyte to a seven-celled/eight-nucleate female gametophyte occurred in the common ancestor of the sister group to Austrobaileyales (a clade that includes monocots, eumagnoliids, and eudicots). Comparative analysis of reconstructed ancestral female gametophyte ontogenies identifies specific early stages of ontogeny that were modified during this transition. These modifications generated two important angiosperm novelties-a set of three persistent antipodal cells and a binucleate central cell, which upon fertilization yields a triploid endosperm. Early angiosperms are anatomically quite diverse in these two features, although triploid endosperm, composed of one paternal genome and two maternal genomes, is a conserved feature of the overwhelming majority of angiosperms.

Embryological evidence for developmental lability during early angiosperm evolution

Recent advances in angiosperm phylogeny reconstruction, palaeobotany and comparative organismic biology have provided the impetus for a major re-evaluation of the earliest phases of the diversification of flowering plants. We now know that within the first fifteen million years of angiosperm history, three major lineages of flowering plants—monocotyledons, eumagnoliids and eudicotyledons—were established, and that within this window of time, tremendous variation in vegetative and floral characteristics evolved. Here I report on a novel type of embryo sac (angiosperm female gametophyte or haploid egg-producing structure) in Amborella trichopoda, the sole member of the most ancient extant angiosperm lineage. This is the first new pattern of embryo sac structure to be discovered among angiosperms in well over half a century. This discovery also supports the emerging view that the earliest phases of angiosperm evolution were characterized by an extensive degree of developmental experimentation and structural lability, and may provide evidence of a critical link to the gymnospermous ancestors of flowering plants.

The evolution of double fertilization and endosperm: an ”historical” perspective

Abstract One hundred years ago, the developmental origin of endosperm from double fertilization was discovered independently by Navashin and Guignard. For much of the twentieth century, specific events related to the evolutionary origin of the endosperm of flowering plants remained a mystery. However, during the past 20 years, advances in phylogenetic reconstruction of seed plants, genetic theory associated with kin selection, and comparative study of the reproductive biology of the closest living relatives of angiosperms (Gnetales) have advanced our understanding of the evolutionary events associated with the origin of double fertilization and endosperm. Recent developmental analyses of Ephedra and Gnetum (members of Gnetales) indicate that these nonflowering seed plants undergo a regular process of double fertilization that yields two diploid zygotes. Use of explicit genetic and developmental criteria for analysis of evolutionary homology demonstrates congruence with the hypothesis that double fertilization processes in Gnetales and angiosperms were inherited from a common ancestor of the two lineages. In its rudimentary form, the second fertilization event in the ancestors of flowering plants yielded a supernumerary diploid embryo that was genetically identical to the normal embryo, a process most similar to what occurs in extant Ephedra. Subsequent to the divergence of the angiosperm stem lineage, the supernumerary embryo derived from double fertilization was developmentally modified into an embryo-nourishing structure, endosperm, that now characterizes angiosperms.

Evolution of Endosperm Developmental Patterns among Basal Flowering Plants

A phylogenetically based comparative investigation of endosperm development was undertaken in a sample of 13 basal angiosperm taxa. The specific goals were to (1) provide a full developmental analysis of all aspects of endosperm in each species, (2) compare patterns among taxa to determine phylogenetic character distribution, (3) reconstruct the ancestral developmental pattern for angiosperms, and (4) explore scenarios of ontogenetic evolution that occurred during the early radiation of flowering plants. Five taxa, Acorus calamus, Cabomba caroliniana, Ceratophyllum demersum, Drimys winteri, and Platanus racemosa, are described in detail. Data from an additional eight taxa were analyzed and compared with these five. Endosperm ontogeny can be conceived of as a series of stages (characters) during which differential patterns of development occur among taxa (character states). We discovered that differential developmental fate of chalazal and micropylar domains is a common pattern among the endosperms of all basal angiosperm taxa and suggest that this may be a feature of endosperm development in all angiosperms. Differential development of chalazal and micropylar domains in endosperm in basal angiosperms also bears a marked similarity to what occurs in angiosperm embryos. This may have implications for understanding the evolutionary origin of endosperm. Basal angiosperms also exhibit variable endosperm developmental characters, indicating that significant ontogenetic transformation occurred during the early radiation of the clade, although magnoliid taxa exhibit a high degree of conservation in endosperm characters. Identification of the roles of the division of the primary endosperm nucleus and subsequent development of the chalazal and micropylar domains provides the first insight into how different endosperm developmental patterns are evolutionarily and developmentally related.

Female gametophyte and early seed development in Peperomia (Piperaceae)

The evolution of female gametophyte development provides an example of how minor ontogenetic modifications can impact the functional biology of seeds. Mature Peperomia-type female gametophytes are normally depicted as 16-nucleate, nine-celled structures. However, recent ultrastructural data have demonstrated that many previous reports were incorrect, suggesting that our understanding of the Peperomia-type ontogeny is incomplete. In this investigation, female gametophyte and early seed development is described in Peperomia dolabriformis, P. jamesoniana, and P. hispidula. Nuclear positioning, nuclear division, and vacuole morphology are documented during the syncytial stages of development, and two mature female gametophyte cellular configurations are described. Endosperm ploidy is measured in each species using microspectrofluorometry. We conclude that a 10-celled construction is likely the most common cellular configuration in Peperomia and that a three-celled female gametophyte exists in P. hispidula. We also describe how developmental modifications of wall formation could produce the diverse cellular configurations observed throughout Peperomia. Interestingly, the onset of female gametophyte diversification within Piperales correlates with the origin of the perisperm in the common ancestor of Piperaceae + Saururaceae. We posit that the origin of the perisperm may have relaxed selection on endosperm genetic constructs, thereby promoting diversification of female gametophyte ontogeny.

Developmental Evolution of the Sexual Process in Ancient Flowering Plant Lineages

Recent investigations of ancient angiosperm lineages are yielding data critical to a fundamental reassessment of the origin and early evolution of flowering plants. To “reconstruct” the reproductive features of the earliest flowering plants, biological characters must be examined in an

MODULARITY OF THE ANGIOSPERM FEMALE GAMETOPHYTE AND ITS BEARING ON THE EARLY EVOLUTION OF ENDOSPERM IN FLOWERING PLANTS

Abstract The monosporic seven‐celled/eight‐nucleate Polygonumtype female gametophyte has long served as a focal point for discussion of the origin and subsequent evolution of the angiosperm female gametophyte. In Polygonumtype female gametophytes, two haploid female nuclei are incorporated into the central cell, and fusion of a sperm cell with the binucleate central cell produces a triploid endosperm with a complement of two maternal and one paternal genomes, characteristic of most angiosperms. We document the development of a four‐celled/four‐nucleate female gametophyte in Nuphar polysepala (Engelm.) and infer its presence in many other ancient lineages of angiosperms. The central cell of the female gametophyte in these taxa contains only one haploid nucleus; thus endosperm is diploid and has a ratio of one maternal to one paternal genome. Based on comparisons among flowering plants, we conclude that the angiosperm female gametophyte is constructed of modular developmental subunits. Each module is characterized by a common developmental pattern: (1) positioning of a single nucleus within a cytoplasmic domain (pole) of the female gametophyte; (2) two free‐nuclear mitoses to yield four nuclei within that domain; and (3) partitioning of three uninucleate cells adjacent to the pole such that the fourth nucleus is confined to the central region of the female gametophyte (central cell). Within the basal angiosperm lineages Nymphaeales and Illiciales, female gametophytes are characterized by a single developmental module that produces a four‐celled/four‐nucleate structure with a haploid uninucleate central cell. A second pattern, typical of Amborella and the overwhelming majority of eumagnoliids, monocots, and eudicots, involves the early establishment of two developmental modules that produce a seven‐celled/eight‐nucleate female gametophyte with two haploid nuclei in the central cell. Comparative analysis of onto‐genetic sequences suggests that the seven‐celled female gametophyte (two modules) evolved by duplication and ectopic expression of an ancestral Nuphar‐ like developmental module within the chalazal domain of the female gametophyte. These analyses indicate that the first angiosperm female gametophytes were composed of a single developmental module, which upon double fertilization yielded a diploid endosperm. Early in angiosperm history this basic module was duplicated, and resulted in a seven‐celled/eight‐nucleate female gametophyte, which yielded a triploid endosperm with the characteristic 2:1 maternal to paternal genome ratio.

Arbuscular mycorrhizal symbionts in Botrychium (Ophioglossaceae).

Many plant species are characterized by a life cycle with a long-lived, subterranean phase that is completely dependent on mycorrhizal fungal symbionts for fixed carbon. This type of life cycle is both phylogenetically and ecologically widespread and is found in diverse vascular plant lineages from the tropics to subalpine meadows. Here we report on the molecular identities of the arbuscular mycorrhizal fungi associated with the autotrophic and underground mycoheterotrophic life cycle phases of the ferns Botrychium crenulatum and B. lanceolatum. We show that the Glomus taxa found in the mycoheterotrophic life cycle phases of B. crenulatum and B. lanceolatum are also found in conspecific and heterospecific photosynthetic neighboring plants. From our DNA sequence data, we infer carbon flow from photosynthetic plants to mycoheterotrophic plants through shared glomalean fungal networks. Finally, our phylogenetic analyses identify a major Glomus clade that forms associations with mycoheterotrophic life cycle stages of B. crenulatum and B. lanceolatum.