The floral genome: an evolutionary history of gene duplication and shifting patterns of gene expression

Through multifaceted genome-scale research involving phylogenomics, targeted gene surveys, and gene expression analyses in diverse basal lineages of angiosperms, our studies provide insights into the most recent common ancestor of all extant flowering plants. MADS-box gene duplications have played an important role in the origin and diversification of angiosperms. Furthermore, early angiosperms possessed a diverse tool kit of floral genes and exhibited developmental 'flexibility', with broader patterns of expression of key floral organ identity genes than are found in eudicots. In particular, homologs of B-function MADS-box genes are more broadly expressed across the floral meristem in basal lineages. These results prompted formulation of the 'fading borders' model, which states that the gradual transitions in floral organ morphology observed in some basal angiosperms (e.g. Amborella) result from a gradient in the level of expression of floral organ identity genes across the developing floral meristem.     

木兰藤科系统位置评述

木兰藤科(Austrobaileyaceae)含1属2种,是系统学上最孤立的科之一。其花粉类似于最古老的被子植物化石之一:晚白垩世的棒纹粉。最新的分子系统发育研究结果表明,木兰藤科是现存被子植物的基部类群之一,其对于被子植物的起源与早期进化的研究具有重要价值。被子植物(有花植物)的起源和辐射一直是植物学家关注的热点。有关木兰藤科的系统位置一直存在争议。本文对该科系统位置的研究历史与现状进行评述。     

A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma

AIMS: We review literature and present new observations on the differences among three general patterns of aerenchyma origin and their systematic distributions among the flowering plants, and we clarify terminology on root aerenchyma. SCOPE: From our own previous works and some new observations, we have analysed the root cortex in 85 species of 41 families in 21 orders of flowering plants that typically grow in wetlands to determine the characteristic patterns of aerenchyma. FINDINGS: A developmental and structural pattern that we term expansigeny, as manifested by honeycomb aerenchyma, is characteristic of all aquatic basal angiosperms (the Nymphaeales) and basal monocots (the Acorales). Expansigenous aerenchyma develops by expansion of intercellular spaces into lacunae by cell division and cell expansion. Schizogeny and lysigeny, so often characterized in recent reviews as the only patterns of root cortex lacunar formation, are present in most wetland plants, but are clearly not present in the most basal flowering plants. CONCLUSION: We conclude that expansigeny is the basic type of aerenchyma development in roots of flowering plants and that the presence of expansigenous honeycomb aerenchyma in root cortices was fundamental to the success of the earliest flowering plants found in wetland environments.     

Cabomba as a model for studies of early angiosperm evolution

BACKGROUND: The angiosperms, or flowering plants, diversified in the Cretaceous to dominate almost all terrestrial environments. Molecular phylogenetic studies indicate that the orders Amborellales, Nymphaeales and Austrobaileyales, collectively termed the ANA grade, diverged as separate lineages from a remaining angiosperm clade at a very early stage in flowering plant evolution. By comparing these early diverging lineages, it is possible to infer the possible morphology and ecology of the last common ancestor of the extant angiosperms, and this analysis can now be extended to try to deduce the developmental mechanisms that were present in early flowering plants. However, not all species in the ANA grade form convenient molecular-genetic models. SCOPE: The present study reviews the genus Cabomba (Nymphaeales), which shows a range of features that make it potentially useful as a genetic model. We focus on characters that have probably been conserved since the last common ancestor of the extant flowering plants. To facilitate the use of Cabomba as a molecular model, we describe methods for its cultivation to flowering in the laboratory, a novel Cabomba flower expressed sequence tag database, a well-adapted in situ hybridization protocol and a measurement of the nuclear genome size of C. caroliniana. We discuss the features required for species to become tractable models, and discuss the relative merits of Cabomba and other ANA-grade angiosperms in molecular-genetic studies aimed at understanding the origin of the flowering plants.     

Evolution of genome size in the angiosperms

Genome size varies extensively across the flowering plants, which has stimulated speculation regarding the ancestral genome size of these plants and trends in genome evolution. We investigated the evolution of C-values across the angiosperms using a molecular phylogenetic framework and C-values not previously available for crucial basal angiosperms, including Amborella, Illiciaceae, and Austrobaileya. Reconstructions of genome size across the angiosperms and extant gymnosperms indicate that the ancestral genome size for angiosperms is very small (1C ≤ 1.4 pg), in agreement with an earlier analysis of Leitch et al. (1998). Furthermore, a very small genome size (1C ≤ 1.4 pg) is ancestral not only for the angiosperms in general, but also for most major clades of flowering plants, including the monocots and the eudicots. The ancestral genome of core eudicots may also have been very small given that very low 1C-values appear to be ancestral for major clades of core eudicots, such as Caryophyllales, Saxifragales, and asterids. Very large genomes occur in clades that occupy derived positions within the monocots and Santalales.     

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.     

Plant microtubule studies: past and present

Here, I briefly review historical and morphological aspects of plant microtubule studies in land plants. Microtubules are formed from tubulins, and the polymeric configurations appear as singlet, doublet, and triplet microtubules. Doublet microtubules occur in the axoneme of cilia and flagella, and triplet microtubules occur in the basal bodies and centrosomes. Doublet and triplet microtubules are lost in all angiosperms and some gymnosperms that do not possess flagellated sperm. In land plants with flagellated sperm, centriolar centrosomes transform into basal bodies during spermatogenesis. In flowering plants, however, most male gametes (sperm) are conveyed to eggs without the benefit of cilia or flagella; thus, higher plants lack centriolar centrosome and doublet and triplet microtubules. The loss of centriolar centrosomes from the life cycle of flowering plants may have influenced the evolution of the plant microtubule system. Comparison of mitotic apparatuses in basal land plants and flowering plants illuminates the evolutionary transition from the centriolar microtubule system to the acentriolar microtubule system.     

The evolution of embryogeny in seed plants and the developmental origin and early history of endosperm

For almost a century, the formation of endosperm from a second and distinctive fertilization event has been viewed as a unique feature of flowering plants. However, until recently, the evolutionary origin of this unique embryo-nourishing entity remained a mystery. Based upon comparative developmental analysis of reproduction among basal angiosperms and their closest extant relatives, the Gnetales (Ephedra, Gnetum, and Welwitschia), it is possible to construct an explicit hypothesis of the events that led to the evolutionary establishment of double fertilization and endosperm. The formulation of this historical record is derived entirely from and dependent upon the determination of reproductive features that are likely to have characterized the common ancestors of angiosperms and Gnetales. Current evidence is most congruent with the concept that a process of double fertilization first evolved in a common ancestor of the Gnetales and angiosperms. Initially, however, the second fertilization product was diploid and yielded a supernumerary embryo. Subsequent to the divergence of the angiosperm lineage from its closest relatives (which include the Gnetales), modification of the development of the supernumerary embryo (derived from the second fertilization event) led to the establishment of an embryo-nourishing endosperm. Comparative analysis of patterns of embryogeny within Gnetales and angiosperms establishes that embryo development in the ancestors of flowering plants (with a rudimentary process of double fertilization) was ab initio cellular, and not free nuclear, as had previously been assumed. Thus, it is likely that the earliest flowering plants displayed an ab initio cellular pattern of endosperm development, whose expression was inherited from that of the supernumerary embryo of the ancestors of flowering plants.     

The meaning of Darwin's 'abominable mystery'

Charles Darwin's "abominable mystery" has come to symbolize just about all aspects of the origin and early evolution of flowering plants. Yet, there has never been an analysis of precisely what Darwin thought was so abominably mysterious. Here I explicate Darwin's thoughts and frustrations with the fossil record of flowering plants as revealed in correspondence with Joseph Hooker, Gaston de Saporta, and Oswald Heer between 1875 and 1881. I also examine the essay by John Ball that prompted Darwin to write his "abominable mystery" letter to Hooker in July of 1879. Contrary to what is generally believed, Darwin's abominable mystery has little if anything to do with the fossil prehistory of angiosperms, identification of the closest relatives of flowering plants, questions of the homologies (and character transformations) of defining features of flowering plants, or the phylogeny of flowering plants themselves. Darwin's abominable mystery and his abiding interest in the radiation of angiosperms were never driven primarily by a need to understand the literal text of the evolutionary history of flowering plants. Rather, Darwin was deeply bothered by what he perceived to be an abrupt origin and highly accelerated rate of diversification of flowering plants in the mid-Cretaceous. This led Darwin to create speculative arguments for a long, gradual, and undiscovered pre-Cretaceous history of flowering plants on a lost island or continent. Darwin also took refuge in the possibility that a rapid diversification of flowering plants in the mid-Cretaceous might, if real, have a biological explanation involving coevolutionary interactions between pollinating insects and angiosperms. Nevertheless, although generations of plant biologists have seized upon Darwin's abominable mystery as a metaphor for their struggle to understand angiosperm history, the evidence strongly suggests that the abominable mystery is not about angiosperms per se. On the contrary, Darwin's abominable mystery is about his abhorrence that evolution could be both rapid and potentially even saltational. Throughout the last years of his life, it just so happens that flowering plants, among all groups of organisms, presented Darwin with the most extreme exception to his strongly held notion natura non facit saltum, nature does not make a leap.     

腺齿木科系统位置评述

腺齿木科(Trimeniaceae)含2属5种。形态学研究显示腺齿木科具有许多原始性状。最新的分子系统发育研究显示,腺齿木科是现存被子植物的重要基部类群之一。但有关腺齿木科的系统位置存在争议。被子植物(有花植物)的起源与辐射一直是植物系统学家关注的热点。对该科系统位置的研究历史与现状进行评述。     

Phylogenetic tree of vascular plants reveals the origins of aquatic angiosperms

Although aquatic plants are discussed as a unified biological group, they are phylogenetically well dispersed across the angiosperms. In this study, we annotated the aquatic taxa on the tree of vascular plants, and extracted the topology of these aquatic lineages to construct the tree of aquatic angiosperms. We also reconstructed the ancestral areas of aquatic families. We found that aquatic angiosperms could be divided into two different categories: the four aquatic orders and the aquatic taxa in terrestrial orders. Aquatic lineages evolved early in the radiation of angiosperms, both in the orders Nymphaeales and Ceratophyllales and among basal monocots (Acorales and Alismatales). These aquatic orders do not have any extant terrestrial relatives. They originated from aquatic habitats during the Early Cretaceous. Asia would have been one of the centers for early diversification of aquatic angiosperms. The aquatic families within terrestrial orders may originate from other areas besides Asia, such as America or Australia. The lineages leading to extant angiosperms diversified early in underexploited freshwater habitats. The four extant aquatic orders were relicts of an early radiation of angiosperm in aquatic environments. Their extinct ancestors might be aquatic early angiosperms.     

莲科系统位置评述

莲科含1属1种2亚种,以具有最古老的有活力的种子而著称。形态学研究显示,莲不仅具有双子叶植物特征,而且又具有单子叶植物的某些性状。因此,对研究被子植物(有花植物)的起源与演化以及单子叶植物的起源具有重要价值。被子植物(有花植物)的起源与辐射一直是植物学家关注的热点,有关莲科的系统位置存在争议。该文对该科系统位置的研究历史与现状进行评述。     

Organization of the root apical meristem in angiosperms

Although flowers, leaves, and stems of the angiosperms have understandably received more attention than roots, the growing root tips, or root apical meristems (RAMs), are organs that could provide insight into angiosperm evolution. We studied RAM organization across a broad spectrum of angiosperms (45 orders and 132 families of basal angiosperms, monocots, and eudicots) to characterize angiosperm RAMs and cortex development related to RAMs. Types of RAM organization in root tips of flowering plants include open RAMs without boundaries between some tissues in the growing tip and closed RAMs with distinct boundaries between apical regions. Epidermis origin is associated with the cortex in some basal angiosperms and monocots and with the lateral rootcap in eudicots and other basal angiosperms. In most angiosperm RAMs, initials for the central region of the rootcap, or columella, are distinct from the lateral rootcap and its initials. Slightly more angiosperm families have exclusively closed RAMs than exclusively open RAMs, but many families have representatives with both open and closed RAMs. Root tips with open RAMs are generally found in angiosperm families considered sister to other families; certain open RAMs may be ancestral in angiosperms.     

被子植物的起源-以喜花虻类化石为据

喜花昆虫在被子植物的起源和早期演化上起着决定性的作用。虻类化石中的许多类群都有访花习性,它们为研究被子植物的起源提供了独特材料。虽然最老的被子植物化石还没有发现,但是喜花虻类的爆发式出现,表示了被子植物出现的时间和地点。本文主要以欧亚大陆东部,特别是中国辽西的侏罗杨虻类化石为材料,在功能形态分析和与现代类群作对比的基础上,证证实了虻类是显花植物最原始的传粉类群之一。中国东北、哈萨克斯坦和西伯利来晚     

A developmental and evolutionary analysis of embryology in Platanus (platanaceae), abasal eudicot

The Platanaceae are an early derived eudicot lineage and therefore occupy a key position for understanding reproductive character diversification associated with the early evolutionary radiation of flowering plants. We conducted an embryological study of Platanus racemosa in order to provide critical data on defining angiosperm reproductive characters for this important group. Female gametophyte development is monosporic. Embryogenesis occurs in a series of stages including zygote elongation and division, development of a linear proembryo, formation of the embryo proper, histogenesis, organogenesis, and growth. Endosperm development is a complex process that includes four distinct phases: free nuclear proliferation, cellularization of the chalazal zone, centripetal cellularization of the micropylar zone, and cellular differentiation and growth. Only the outer endosperm layer persists at seed maturity. Our findings differ significantly from previously published reports for Platanus, in which endosperm development was described as ab initio cellular. A comparison of endosperm development in Platanus with several closely and distantly related free nuclear taxa reveals considerable developmental variability, consistent with a hypothesis of multiple origins of free nuclear endosperm in angiosperms. Our analysis indicates that much remains to be learned about embryology in basal angiosperms. Additional developmental and comparative studies will likely reveal critical insights into the early evolution of flowering plants.     

睡莲科系统位置评述

形态学研究显示睡莲科Nymphaeaceae具有许多原始性状。睡莲科又被称为“古草本”。最新的分子系统发育研究显示,睡莲科是现存被子植物系统树根部附近最早分异谱系的演化支之一,对研究被子植物(有花植物)的起源与早期进化具有重要价值,但有关睡莲科的范围和系统位置存在争议。被子植物的起源与辐射一直是植物学家关注的热点。本文对该科系统位置的研究历史与现状进行了评述。     

Phylogenetic analysis of the plant-specific zinc finger-homeobox and mini zinc finger gene families

Zinc finger-homeodomain proteins (ZHD) are present in many plants; however, the evolutionary history of the ZHD gene family remains largely unknown. We show here that ZHD genes are plant-specific, nearly all intronless, and related to MINI ZINC FINGER ( MIF ) genes that possess only the zinc finger. Phylogenetic analyses of ZHD genes from representative land plants suggest that non-seed plant ZHD genes occupy basal positions and angiosperm homologs form seven distinct clades. Several clades contain genes from two or more major angiosperm groups, including eudicots, monocots, magnoliids, and other basal angiosperms, indicating that several duplications occurred before the diversification of flowering plants. In addition, specific lineages have experienced more recent duplications. Unlike the ZHD genes, MIF s are found only from seed plants, possibly derived from ZHD s by loss of the homeodomain before the divergence of seed plants. Moreover, the MIF genes have also undergone relatively recent gene duplications. Finally, genome duplication might have contributed substantially to the expansion of family size in angiosperms and caused a high level of functional redundancy/overlap in these genes.     

Multigene analyses identify the three earliest lineages of extant flowering plants

Flowering plants (angiosperms) are by far the largest, most diverse, and most important group of land plants, with over 250,000 species and a dominating presence in most terrestrial ecosystems. Understanding the origin and early diversification of angiosperms has posed a long-standing botanical challenge [1]. Numerous morphological and molecular systematic studies have attempted to reconstruct the early history of this group, including identifying the root of the angiosperm tree. There is considerable disagreement among these studies, with various groups of putatively basal angiosperms from the subclass Magnoliidae having been placed at the root of the angiosperm tree (reviewed in [2-4]). We investigated the early evolution of angiosperms by conducting combined phylogenetic analyses of five genes that represent all three plant genomes from a broad sampling of angiosperms. Amborella, a monotypic, vessel-less dioecious shrub from New Caledonia, was clearly identified as the first branch of angiosperm evolution, followed by the Nymphaeales (water lillies), and then a clade of woody vines comprising Schisandraceae and Austrobaileyaceae. These findings are remarkably congruent with those from several concurrent molecular studies [5-7] and have important implications for whether or not the first angiosperms were woody and contained vessels, for interpreting the evolution of other key characteristics of basal angiosperms, and for understanding the timing and pattern of angiosperm origin and diversification.     

Darwin's second 'abominable mystery': Why are there so many angiosperm species?

The rapid diversification and ecological dominance of the flowering plants beg the question "Why are there so many angiosperm species and why are they so successful?" A number of equally plausible hypotheses have been advanced in response to this question, among which the most widely accepted highlights the mutually beneficial animal-plant relationships that are nowhere better developed nor more widespread than among angiosperm species and their biotic vectors for pollination and dispersal. Nevertheless, consensus acknowledges that there are many other attributes unique to or characteristic of the flowering plants. In addition, the remarkable coevolution of the angiosperms and pollination/dispersal animal agents could be an effect of the intrinsic adaptability of the flowering plants rather than a primary cause of their success, suggesting that the search for underlying causes should focus on an exploration of the genetic and epigenetic mechanisms that might facilitate adaptive evolution and speciation. Here, we explore angiosperm diversity promoting attributes in their general form and draw particular attention to those that, either individually or collectively, have been shown empirically to favor high speciation rates, low extinction rates, or broad ecological tolerances. Among these are the annual growth form, homeotic gene effects, asexual/sexual reproduction, a propensity for hybrid polyploidy, and apparent "resistance" to extinction. Our survey of the literature suggests that no single vegetative, reproductive, or ecological feature taken in isolation can account for the evolutionary success of the angiosperms. Rather, we believe that the answer to Darwin's second "abominable mystery" lies in a confluence of features that collectively make the angiosperms unique among the land plants.