Perspective: the origin of flowering plants and their reproductive biology--a tale of two phylogenies

Recently, two areas of plant phylogeny have developed in ways that could not have been anticipated, even a few years ago. Among extant seed plants, new phylogenetic hypotheses suggest that Gnetales, a group of nonflowering seed plants widely hypothesized to be the closest extant relatives of angiosperms, may be less closely related to angiosperms than was believed. In addition, recent phylogenetic analyses of angiosperms have, for the first time, clearly identified the earliest lineages of flowering plants: Amborella, Nymphaeales, and a clade that includes Illiciales/ Trimeniaceae/Austrobaileyaceae. Together, the new seed plant and angiosperm phylogenetic hypotheses have major implications for interpretation of homology and character evolution associated with the origin and early history of flowering plants. As an example of the complex and often unpredictable interplay of phylogenetic and comparative biology, we analyze the evolution of double fertilization, a process that forms a diploid embryo and a triploid endosperm, the embryo-nourishing tissue unique to flowering plants. We demonstrate how the new phylogenetic hypotheses for seed plants and angiosperms can significantly alter previous interpretations of evolutionary homology and firmly entrenched assumptions about what is synapomorphic of flowering plants. In the case of endosperm, a solution to the century-old question of its potential homology with an embryo or a female gametophyte (the haploid egg-producing generation within the life cycle of a seed plant) remains complex and elusive. Too little is known of the comparative reproductive biology of extant nonflowering seed plants (Gnetales, conifers, cycads, and Ginkgo) to analyze definitively the potential homology of endosperm with antecedent structures. Remarkably, the new angiosperm phylogenies reveal that a second fertilization event to yield a biparental endosperm, long assumed to be an important synapomorphy of flowering plants, cannot be conclusively resolved as ancestral for flowering plants. Although substantive progress has been made in the analysis of phylogenetic relationships of seed plants and angiosperms, these efforts have not been matched by comparable levels of activity in comparative biology. The consequence of inadequate comparative biological information in an age of phylogenetic biology is a severe limitation on the potential to reconstruct key evolutionary historical events.     

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

 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. Received: 25 September 1997 / Accepted: 3 November 1997     

Developmental and evolutionary hypotheses for the origin of double fertilization and endosperm.

The discovery of a second fertilization event that initiates endosperm in flowering plants, just over a century ago, stimulated intense interest in the evolutionary history and homology of endosperm, the genetically biparental embryo-nourishing tissue that is found only in angiosperms. Two alternative hypotheses for the origin of double fertilization and endosperm have been invoked to explain the origin of the angiosperm reproductive syndrome from a typical non-flowering seed plant reproductive syndrome. Endosperm may have arisen from a developmental transformation of a supernumerary embryo derived from a rudimentary second fertilization event that first evolved in the ancestors of angiosperms (endosperm homologous with an embryo). Conversely, endosperm may represent the developmental transformation of the cellular phase of non-flowering seed plant female gametophyte ontogeny that was later sexualized by the addition of a second fertilization event in a strongly progenetic female gametophyte (endosperm homologous with a female gametophyte). For the first time, explicit developmental and evolutionary transitions for both of these hypotheses are examined and compared. In addition, current data that may be congruent with either of these hypotheses are discussed. It is clear that much remains to be accomplished if the evolutionary significance of the process of double fertilization and the formation of endosperm is to be fully understood.     

A model of triploid endosperm evolution driven by parent-offspring conflict

The parental investment in angiosperms comprises the endosperm, a nutrient reserve that is used during seed development. The endosperm contains genes from both parents. The most common endosperm form is the 3n Polygonum -type with more maternal genetic influence than paternal, i.e. with two maternal nuclei and one paternal nucleus. The evolutionary original state is thought to be a diploid endosperm with equal influence of the parents. We focus on the evolution of the triploid endosperm and show that a gene for triploid endosperm would have an initial advantage in a population of diploid endosperm type plants, and increase to fixation. We assume that endosperm amount is controlled by endosperm genes. Then a gene causing triploid endosperm will increase the influence of the mother plant on parental investment. The production of endosperm with two copies of the maternal genes will modify the inheritance of endosperm amount and cause an increased production of seeds.     

Endosperm: food for humankind and fodder for scientific discoveries

The endosperm is an essential constituent of seeds in flowering plants. It originates from a fertilization event parallel to the fertilization that gives rise to the embryo. The endosperm nurtures embryo development and, in some species including cereals, stores the seed reserves and represents a major source of food for humankind. Endosperm biology is characterized by specific features, including idiosyncratic cellular controls of cell division and epigenetic controls associated with parental genomic imprinting. This review attempts a comprehensive summary of our current knowledge of endosperm development and highlights recent advances in this field.     

Modelling epistatic effects of embryo and endosperm QTL on seed quality traits

Coordinated expression of embryo and endosperm tissues is required for proper seed development. The coordination among these two tissues is controlled by the interaction between multiple genes expressed in the embryo and endosperm genomes. In this article, we present a statistical model for testing whether quantitative trait loci (QTL) active in different genomes, diploid embryo and triploid endosperm, epistatically affect a trait expressed on the endosperm tissue. The maximum likelihood approach, implemented with the EM algorithm, was derived to provide the maximum likelihood estimates of the locations of embryo- and endosperm-specific QTL and their main effects and epistatic effects. This model was used in a real example for rice in which two QTL, one from the embryo genome and the other from the endosperm genome, exert a significant interaction effect on gel consistency on the endosperm. Our model has successfully detected Waxy, a candidate gene in the embryo genome known to regulate one of the major steps of amylose biosynthesis in the endosperm. This model will have great implications for agricultural and evolutionary genetic research.     

Epigenetic mechanisms in the endosperm and their consequences for the evolution of flowering plants

The sudden rise of angiosperms to ecological dominance was an "abominable mystery" to Charles Darwin, and understanding the underlying evolutionary driving force has remained a scientific challenge since then. The recognition of polyploidization as an important factor for plant speciation is likely to hold a key to this mystery and we will discuss possible mechanisms underlying this phenomenon. Polyploidization raises an immediate reproductive barrier in the endosperm, pointing towards an important but greatly underestimated role of the endosperm in preventing interploidy hybridizations. Parent-of-origin-specific gene expression is largely restricted to the endosperm, providing an explanation for the dosage sensitivity of the endosperm. Here, we review epigenetic mechanisms causing endosperm dosage sensitivity, their possible consequences for raising interploidy and interspecies hybridization barriers and their impact on flowering plant evolution. This article is part of a Special Issue entitled: Epigenetic Control.     

Endosperm: the crossroad of seed development

The endosperm is an essential part of the seed that sustains embryo development and reserve storage. Several genes that are involved in endosperm differentiation and that have domains of expression arranged along a conserved antero-posterior axis have been isolated in Arabidopsis and in cereals. Endosperm polarity is controlled maternally by chromatin-remodeling complexes. Endosperm development appears to be predominantly under epigenetic controls that might be linked with its evolutionary origin.     

五针松胚乳ISSR-PCR反应体系的建立

采用改良的CTAB法提取5种五针松胚乳DNA,经检测,该方法提取的DNA纯度和含量较高,单粒种子胚乳DNA得率基本满足大量PCR扩增的需要。建立了稳定的、可重复的五针松ISSR-PCR最佳反应体系及PCR扩增程序,筛选出了扩增条带清晰、多态性丰富的16个ISSR引物,为今后利用五针松种子胚乳开展遗传图谱构建等分子生物学研究提供一个标准化程序。     

Embryology in Trithuria submersa (Hydatellaceae) and relationships between embryo, endosperm, and perisperm in early-diverging flowering plants

? Premise of the study: Despite their highly reduced morphology, Hydatellaceae bear the unmistakable embryological signature of Nymphaeales, including a starch-rich maternal perisperm and a minute biparental endosperm and embryo. The co-occurrence of perisperm and endosperm in Nymphaeales and other lineages of flowering plants, and their respective functions during the course of seed development and embryo germination, remain enigmatic. ? Methods: Development of the embryo, endosperm, and perisperm was examined histologically from fertilization through germination in flowers and fruits of Trithuria submersa. ? Key results: The embryo of T. submersa initiates two cotyledons prior to seed maturity/dormancy, and their tips remain in contact with the endosperm throughout germination. The endosperm persists as a single layer of cells and serves as the interface between the embryo and the perisperm. The perisperm contains carbohydrates and proteins, and functions as the main storage tissue. The endosperm accumulates proteins and aleurone grains and functions as a transfer cell layer. ? Conclusions: In Nymphaeales, the multiple roles of a more typical endosperm have been separated into two different tissues and genetic entities: a maternal perisperm (nutrient acquisition, storage, mobilization) and a minute biparental endosperm (nutrient transfer to the embryo). The presence of perisperms among several other ancient lineages of angiosperms suggests a modest degree of developmental and functional lability for the nutrient storage tissue (perisperm or endosperm) within seeds during the early evolution of flowering plants. Finally, we examine the evolutionary developmental hypothesis that, contrary to longstanding assumptions, an embryo-nourishing perisperm along with a minute endosperm may represent the plesiomorphic condition for flowering plants.     

Endosperm development in the Araceae (Alismatales) and evolution of developmental modes in monocots

The Araceae, a basal-most family of Alismatales that basally diverged subsequent to Acorales in monocot phylogeny, are known to have diverse modes of endosperm development: nuclear, helobial, and cellular. However, the occurrence of nuclear and helobial endosperm development has long been debated. Here, we report a (re-)investigation of endosperm development in Lysichiton, Orontium, and Symplocarpus of the Orontioideae (a basal Araceae), in which nuclear endosperm development was recorded more than 100 years ago. The results show that all three genera exhibit a cellular, rather than nuclear, endosperm development and suggest that the helobial endosperm development reported as an “unmistakable record” from Ariopsis is likely cellular. Thus the Araceae are very likely characterized by cellular endosperm development alone. An extensive comparison with other monocots in light of phylogenetic relationships demonstrates that a plesiomorphic cellular endosperm development is restricted to the three basal monocot orders Acorales, Alismatales, and Petrosaviales, in which evolutionary changes from cellular to nuclear endosperm development occurred twice as major events, once within Alismatales and once as a synapomorphy of the eight remaining monocot orders, including Dioscoreales, Liliales, Asparagales, and Poales, and that helobial endosperm development, which is known for many monocot families, evolved as homoplasy throughout the monocots.     

Embryology of Manekia naranjoana (Piperaceae) and the origin of tetrasporic, 16-nucleate female gametophytes in Piperales

The vast majority of flowering plant seeds contain a triploid endosperm formed by fertilization of a monosporic, Polygonum-type female gametophyte. However, evolutionary transitions to six other genetic constructs of endosperm are widespread, and six of seven known patterns are found in the order Piperales. Within Piperaceae, Manekia has not been described, and we report its female gametophyte to be tetrasporic and 16-nucleate at maturity. Manekia ontogeny is generally characterized by early establishment of a bipolar or weakly bipolar body plan and a binucleate central cell at maturity (Drusa-type pattern); however, ca. 16% of early stages had distinctly tetrapolar organization, and ca. 21% of mature specimens had a tetranucleate central cell (Penaea-type pattern, not previously reported in Piperaceae). An evolutionary developmental analysis indicates heterochrony, heterotopy, novelties, and sequence deletions have each played roles in modulating variation within Piperales. Our data suggest the common ancestor of Piperaceae was tetrasporic and retained a plesiomorphic bipolar body plan, producing a "functionally bisporic" form of triploid endosperm derived from the lineal descendants of two megaspores and a sperm. Developmental modifications of this tetrasporic, bipolar ontogeny can account for the origin of all three other known "true" tetrasporic endosperm genetic constructs, formed from derivatives of all four megaspores and a sperm. These derived endosperms in turn have higher ploidy, higher potential heterozygosity, and reduced genetic conflicts.     

Evolutionary developmental biology its roots and characteristics

The rise of evolutionary developmental biology was not the progressive isolation and characterization of developmental genes and gene networks. Many obstacles had to be overcome: the idea that all genes were more or less involved in development; the evidence that developmental processes in insects had nothing in common with those of vertebrates.Different lines of research converged toward the creation of evolutionary developmental biology, giving this field of research its present heterogeneity. This does not prevent all those working in the field from sharing the conviction that a precise characterization of evolutionary variations is required to fully understand the evolutionary process.Some evolutionary developmental biologists directly challenge the Modern Synthesis. I propose some ways to reconcile these apparently opposed visions of evolution. The turbulence seen in evolutionary developmental biology reflects the present entry of history into biology.     

Popper, falsifiability, and evolutionary biology

First, a brief history is provided of Popper's views on the status of evolutionary biology as a science. The views of some prominent biologists are then canvassed on the matter of falsifiability and its relation to evolutionary biology. Following that, I argue that Popper's programme of falsifiability does indeed exclude evolutionary biology from within the circumference of genuine science, that Popper's programme is fundamentally incoherent, and that the correction of this incoherence results in a greatly expanded and much more realistic concept of what is empirical, resulting in the inclusion of evolutionary biology. Finally, this expanded concept of empirical is applied to two particular problems in evolutionary biology — viz., the species problem and the debate over the theory of punctuated equilibria — and it is argued that both of them are still mainly metaphysical.     

Evolutionary Novelty and the Evo-Devo Synthesis: Field Notes

Accounting for the evolutionary origins of morphological novelty is one of the core challenges of contemporary evolutionary biology. A successful explanatory framework requires the integration of different biological disciplines, but the relationships between developmental biology and standard evolutionary biology remain contested. There is also disagreement about how to define the concept of evolutionary novelty. These issues were the subjects of a workshop held in November 2009 at the University of Alberta. We report on the discussion and results of this workshop, addressing questions about (i) how to define evolutionary novelty and understand its significance, (ii) how to interpret evolutionary developmental biology as a synthesis and its relation to neo-Darwinian evolutionary theory, and (iii) how to integrate disparate biological approaches in general.     

鹅观草属一些种种子胚乳细胞的特征及其分类学意义的探讨

解剖观察了鹅观草属１８个种的胚乳细胞,发现这此细胞在鹅观草属各类群间的发育是不同步的,其中胚乳细胞的大小、形状、数量以及反映丰厚程度的长宽比不仅具有类群鉴分的价值,而且还可作为推证类群演化关系的旁证。分析结果表明,胚乳细胞体积的增大。数量的增多、细胞的变圆、长宽幽会的减少皆与类群的进化趋势相顺应。据此,进一步阐述了鹅观草属组、系、种的系统发育关系。     

The structure of microbial evolutionary theory

The study of microbial phylogeny and evolution has emerged as an interdisciplinary synthesis, divergent in both methods and concepts from the classical evolutionary biology. The deployment of macromolecular sequencing in microbial classification has provided a deep evolutionary taxonomy hitherto deemed impossible. Microbial phylogenetics has greatly transformed the landscape of evolutionary biology, not only in revitalizing the field in the pursuit of life's history over billions of years, but also in transcending the structure of thought that has shaped evolutionary theory since the time of Darwin. A trio of primary phylogenetic lineages, along with the recognition of symbiosis and lateral gene transfer as fundamental processes of evolutionary innovation, are core principles of microbial evolutionary biology today. Their scope and significance remain contentious among evolutionists.     

Seed germination and dormancy: The classic story,new puzzles,and evolution

This review highlights recent progresses in seed germination and dormancy research.Research on the weakening of the endosperm during germination,which is almost a classic theme in seed biology,was resumed byα-xylosidase studies.Strong genetic evidence was presented to suggest that the quality control of xyloglucan biosynthesis in the endosperm(and the embryo)plays a critical role in germination.Further analyses on the endosperm and the adjace nt layers have suggested that the cutin coat in the endosperm-testa interphase negatively affects germination while the en dosperm-embryo in terphase produces a sheath that facilitates germination.These progresses significantly advanced our understanding of seed germination mechanisms.A breakthrough in dormancy research,on the other hand,revealed the unique abscisic acid signaling pathway that is regulated by DELAY OF GERMINATION1(DOG1).The detailed analysis of DOC1 expression uncovered the intriguing story of reciprocal regulation of the sensean tisense pair,which gen erated new questions.Recent studies also suggested that the DOG1 function is not limited to dormancy but extended through general seed maturation,which provokes questions about the evolution of DOG1 family proteins.Seed biology is becoming more exciting with the classic stories being revitalized and new puzzles emerging from the frontier.     

Examining the Interaction of Acceptance and Understanding: How Does the Relationship Change with a Focus on Macroevolution?

The goal of this research was to illuminate the relationship between students’ acceptance and understanding of macroevolution. Our research questions were: (1) Is there a relationship between knowledge of macroevolution and acceptance of the theory of evolution?; (2) Is there a relationship between the amount of college level biology course work and acceptance of evolutionary theory and knowledge of macroevolution?; and (3) Can college student acceptance of the theory of evolution and knowledge of macroevolution change over the course of a semester? The research participants included 667 students from a first-semester biology course and 74 students from the evolutionary biology course. Data were collected using both the MATE (a measure of the acceptance of evolutionary theory) and the MUM (a measure of understanding of macroevolution). Pre-instruction data were obtained for the introductory biology course, and pre- and post-data were obtained for the evolutionary biology course. Analysis revealed acceptance of evolution (as measured by the MATE) was correlated to understanding of macroevolution, and the number of biology courses was significantly correlated to acceptance and knowledge of macroevolution. Finally, there was a statistically significant change in students’ understanding of macroevolution and acceptance of evolution after the one-semester evolutionary biology course. Significance of these findings is discussed.