Angiosperms are the largest and most successful clade of land plants with >250,000 species distributed in nearly every terrestrial habitat. Many phylogenetic studies have been based on DNA sequences of one to several genes, but, despite decades of intensive efforts, relationships among early diverging lineages and several of the major clades remain either incompletely resolved or weakly supported. We performed phylogenetic analyses of 81 plastid genes in 64 sequenced genomes, including 13 new genomes, to estimate relationships among the major angiosperm clades, and the resulting trees are used to examine the evolution of gene and intron content. Phylogenetic trees from multiple methods, including model-based approaches, provide strong support for the position of Amborella as the earliest diverging lineage of flowering plants, followed by Nymphaeales and Austrobaileyales. The plastid genome trees also provide strong support for a sister relationship between eudicots and monocots, and this group is sister to a clade that includes Chloranthales and magnoliids. Resolution of relationships among the major clades of angiosperms provides the necessary framework for addressing numerous evolutionary questions regarding the rapid diversification of angiosperms. Gene and intron content are highly conserved among the early diverging angiosperms and basal eudicots, but 62 independent gene and intron losses are limited to the more derived monocot and eudicot clades. Moreover, a lineage-specific correlation was detected between rates of nucleotide substitutions, indels, and genomic rearrangements. angiosperm evolution ͉ molecular evolution A ngiosperms, the largest clade of land plants with Ͼ250,000 species, experienced rapid radiation soon after their first appearance in the fossil record (1). As a result, flowering plants exhibit incredible diversity in habit, morphology, anatomy, physiology, and reproductive biology. This variation has presented major challenges to biologists interested in the origin and evolution of these traits, and resolving these issues critically depends on having a well resolved and strongly supported phylogenetic framework. Over the past 20 years, numerous phylogenetic studies have used both morphological and molecular data to assess relationships among the major clades (reviewed in ref.2), resulting in a widely accepted classification of angiosperms with 45 orders and 457 families (3).For nearly two decades, most phylogenetic analyses of angiosperms have relied on DNA sequences of one to several genes from the plastid, mitochondrial, and nuclear genomes (reviewed in ref.2). Despite these intensive efforts there are still uncertainties regarding relationships among several major clades throughout angiosperms, including the earliest diverging lineages. Recent studies support the placement of Amborella sister to all remaining angiosperms, but support is often low. Amborella has also been placed with waterlilies (Nymphaeales) in a clade sister to other angiosperms (4-7). In many studies, resolution of r...
Background: The number of completely sequenced plastid genomes available is growing rapidly. This array of sequences presents new opportunities to perform comparative analyses. In comparative studies, it is often useful to compare across wide phylogenetic spans and, within angiosperms, to include representatives from basally diverging lineages such as the genomes reported here: Nuphar advena (from a basal-most lineage) and Ranunculus macranthus (a basal eudicot). We report these two new plastid genome sequences and make comparisons (within angiosperms, seed plants, or all photosynthetic lineages) to evaluate features such as the status of ycf15 and ycf68 as protein coding genes, the distribution of simple sequence repeats (SSRs) and longer dispersed repeats (SDR), and patterns of nucleotide composition.
During the past decade, there has been a rapid increase in our understanding of plastid genome organization and evolution due to the availability of many new completely sequenced genomes. There are 45 complete genomes published and ongoing projects are likely to increase this sampling to nearly 200 genomes during the next 5 years. Several groups of researchers including ours have been developing new techniques for gathering and analyzing entire plastid genome sequences and details of these developments are summarized in this chapter. The most important developments that enhance our ability to generate whole chloroplast genome sequences involve the generation of pure fractions of chloroplast genomes by whole genome amplification using rolling circle amplification, cloning genomes into Fosmid or bacterial artificial chromosome (BAC) vectors, and the development of an organellar annotation program (Dual Organellar GenoMe Annotator [DOGMA]). In addition to providing details of these methods, we provide an overview of methods for analyzing complete plastid genome sequences for repeats and gene content, as well as approaches for using gene order and sequence data for phylogeny reconstruction. This explosive increase in the number of sequenced plastid genomes and improved computational tools will provide many insights into the evolution of these genomes and much new data for assessing relationships at deep nodes in plants and other photosynthetic organisms.
While there has been strong support for Amborella and Nymphaeales (water lilies) as branching from basal-most nodes in the angiosperm phylogeny, this hypothesis has recently been challenged by phylogenetic analyses of 61 protein-coding genes extracted from the chloroplast genome sequences of Amborella, Nymphaea, and 12 other available land plant chloroplast genomes. These character-rich analyses placed the monocots, represented by three grasses (Poaceae), as sister to all other extant angiosperm lineages. We have extracted protein-coding regions from draft sequences for six additional chloroplast genomes to test whether this surprising result could be an artifact of long-branch attraction due to limited taxon sampling. The added taxa include three monocots (Acorus, Yucca, and Typha), a water lily (Nuphar), a ranunculid (Ranunculus), and a gymnosperm (Ginkgo). Phylogenetic analyses of the expanded DNA and protein data sets together with microstructural characters (indels) provided unambiguous support for Amborella and the Nymphaeales as branching from the basal-most nodes in the angiosperm phylogeny. However, their relative positions proved to be dependent on the method of analysis, with parsimony favoring Amborella as sister to all other angiosperms and maximum likelihood (ML) and neighbor-joining methods favoring an Amborella + Nymphaeales clade as sister. The ML phylogeny supported the later hypothesis, but the likelihood for the former hypothesis was not significantly different. Parametric bootstrap analysis, single-gene phylogenies, estimated divergence dates, and conflicting indel characters all help to illuminate the nature of the conflict in resolution of the most basal nodes in the angiosperm phylogeny. Molecular dating analyses provided median age estimates of 161 MYA for the most recent common ancestor (MRCA) of all extant angiosperms and 145 MYA for the MRCA of monocots, magnoliids, and eudicots. Whereas long sequences reduce variance in branch lengths and molecular dating estimates, the impact of improved taxon sampling on the rooting of the angiosperm phylogeny together with the results of parametric bootstrap analyses demonstrate how long-branch attraction might mislead genome-scale phylogenetic analyses.
This chapter focuses on two aspects of the plant chloroplast genome: (i) its organization and evolution; and (ii) the phylogenetic utility of different approaches to cpDNA characterization.
Two groups of extant plants, lycopsids and psilopsids, alternatively have been suggested to be the living representatives of the earliest diverging lineage in vascular plant evolution. The chloroplast DNA (cpDNA) gene order is known to contain an inversion in bryophytes and tracheophytes relative to one another. Characterization of tracheophyte cpDNAs shows that lycopsids share the gene order with bryophytes, whereas all other vascular plants share the inverted gene order. The distribution of this character provides strong support for the fundamental nature of the phylogenetic separation of lycopsids and marks the ancient evolutionary split in early vascular land plants.
Campanulaceae are a large, nearly cosmopolitan angiosperm family that are well‐accepted as monophyletic but whose intrafamilial and intrageneric relationships are controversial. We used DNA sequences of the chloroplast genes atpB, matK, and rbcL to infer the phylogeny of 102 taxa in 41 genera plus four outgroup taxa. Our sampling represents a wide taxonomic and geographic diversity from within the family. Results from maximum parsimony and Bayesian analyses provide strong evidence for two major clades in the family, with the platycodonoids sister to the remaining members of the family, the wahlenbergioids and campanuloids. There are two clear divisions within the campanuloids that correspond well with the historical Campanula s.str. and Rapunculus groups of Boissier and Fedorov. The phylogenetic positions of the Northern European species Wahlenbergia hederacea and the genus Jasione remain unresolved. Our results also provide evidence that the large, inclusive genera Wahlenbergia and Campanula are polyphyletic, and the smaller, segregate genera Symphyandra, Prismatocarpus, and Legousia are not monophyletic. Insights are provided into the different biogeographic origins of several oceanic island endemics. Heterochaenia, Nesocodon, and Berenice occur in a single clade, which suggests a single colonization of the Indian Ocean Mascarene Islands. Conversely, Wahlenbergia linifolia and W. angustifolia of St. Helena Island in the mid‐Atlantic are not sister taxa. The Macaronesian taxa, Canarina canariensis, and Musschia aurea, which display convergent bird‐pollination adaptations and with Azorina vidalii of the Azores, woody growth form, fall into separate major lineages. The North American Campanulaceae also do not form a monophyletic group, providing evidence that these taxa are the descendents of multiple introductions onto the North American continent.
Obtaining accurate phylogenies and effective species discrimination using a small standardized set of plastid genes is challenging in evolutionarily young lineages. Complete plastid genome sequencing offers an increasingly easy-to-access source of characters that helps address this. The usefulness of this approach, however, depends on the extent to which plastid haplotypes track morphological species boundaries. We have tested the power of complete plastid genomes to discriminate among multiple accessions of 11 of 13 New Caledonian Araucaria species, an evolutionarily young lineage where the standard DNA barcoding approach has so far failed and phylogenetic relationships have remained elusive. Additionally, 11 nuclear gene regions were Sanger sequenced for all accessions to ascertain the success of species discrimination using a moderate number of nuclear genes. Overall, fewer than half of the New Caledonian Araucaria species with multiple accessions were monophyletic in the plastid or nuclear trees. However, the plastid data retrieved a phylogeny with a higher resolution compared to any previously published tree of this clade and supported the monophyly of about twice as many species and nodes compared to the nuclear data set. Modest gains in discrimination thus are possible, but using complete plastid genomes or a small number of nuclear genes in DNA barcoding may not substantially raise species discriminatory power in many evolutionarily young lineages. The big challenge therefore remains to develop techniques that allow routine access to large numbers of nuclear markers scaleable to thousands of individuals from phylogenetically disparate sample sets.
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