The origin of the flower was a key innovation in the history of complex organisms, dramatically altering Earth’s biota. Advances in phylogenetics, developmental genetics, and genomics during the past 25 years have substantially advanced our understanding of the evolution of flowers, yet crucial aspects of floral evolution remain, such as the series of genetic and morphological changes that gave rise to the first flowers; the factors enabling the origin of the pentamerous eudicot flower, which characterizes ∼70% of all extant angiosperm species; and the role of gene and genome duplications in facilitating floral innovations. A key early concept was the ABC model of floral organ specification, developed by Elliott Meyerowitz and Enrico Coen and based on two model systems, Arabidopsis thaliana and Antirrhinum majus. Yet it is now clear that these model systems are highly derived species, whose molecular genetic-developmental organization must be very different from that of ancestral, as well as early, angiosperms. In this article, we will discuss how new research approaches are illuminating the early events in floral evolution and the prospects for further progress. In particular, advancing the next generation of research in floral evolution will require the development of one or more functional model systems from among the basal angiosperms and basal eudicots. More broadly, we urge the development of “model clades” for genomic and evolutionary-developmental analyses, instead of the primary use of single “model organisms.” We predict that new evolutionary models will soon emerge as genetic/genomic models, providing unprecedented new insights into floral evolution.
One contribution of 17 to a theme issue 'Evo-devo in the genomics era, and the origins of morphological diversity'. A salient feature of flowering plant diversification is the emergence of a novel suite of floral features coinciding with the origin of the most species-rich lineage, Pentapetalae. Advances in phylogenetics, developmental genetics and genomics, including new analyses presented here, are helping to reconstruct the specific evolutionary steps involved in the evolution of this clade. The enormous floral diversity among Pentapetalae appears to be built on a highly conserved ground plan of five-parted (pentamerous) flowers with whorled phyllotaxis. By contrast, lability in the number and arrangement of component parts of the flower characterize the early-diverging eudicot lineages subtending Pentapetalae. The diversification of Pentapetalae also coincides closely with ancient hexaploidy, referred to as the gamma whole-genome triplication, for which the phylogenetic timing, mechanistic details and molecular evolutionary consequences are as yet not fully resolved. Transcription factors regulating floral development often persist in duplicate or triplicate in gamma-derived genomes, and both individual genes and whole transcriptional programmes exhibit a shift from broadly overlapping to tightly defined expression domains in Pentapetalae flowers. Investigations of these changes associated with the origin of Pentapetalae can lead to a more comprehensive understanding of what is arguably one of the most important evolutionary diversification events within terrestrial plants.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.
Premise of the study:The use of genome skimming allows systematists to quickly generate large data sets, particularly of sequences in high abundance (e.g., plastomes); however, researchers may be overlooking data in low abundance that could be used for phylogenetic or evo-devo studies. Here, we present a bioinformatics approach that explores the low-abundance portion of genome-skimming next-generation sequencing libraries in the fan-flowered Goodeniaceae.Methods:Twenty-four previously constructed Goodeniaceae genome-skimming Illumina libraries were examined for their utility in mining low-copy nuclear genes involved in floral symmetry, specifically the CYCLOIDEA (CYC)-like genes. De novo assemblies were generated using multiple assemblers, and BLAST searches were performed for CYC1, CYC2, and CYC3 genes.Results:Overall Trinity, SOAPdenovo-Trans, and SOAPdenovo implementing lower k-mer values uncovered the most data, although no assembler consistently outperformed the others. Using SOAPdenovo-Trans across all 24 data sets, we recovered four CYC-like gene groups (CYC1, CYC2, CYC3A, and CYC3B) from a majority of the species. Alignments of the fragments included the entire coding sequence as well as upstream and downstream regions.Discussion:Genome-skimming data sets can provide a significant source of low-copy nuclear gene sequence data that may be used for multiple downstream applications.
BackgroundShifts in floral form across angiosperms, particularly from radially symmetrical to bilaterally symmetrical flowers, are often associated with shifts in speciation rates and changes in pollination syndrome. Growing evidence across both rosids and asterids indicates that CYCLOIDEA (CYC)-like transcription factors from the TCP gene family play a role in establishing the dorsoventral pattern of flower symmetry, which affects the development of both the corolla and androecium. Previous studies of CYC-like genes, especially of the CYC2 clade, indicate that these genes are dorsally restricted in bilaterally symmetrical flowers. Also, gene duplication of CYC-like genes often correlates with shifts in floral form in both individual flowers and head-like inflorescences (capitula).ResultsHere, we compared the expression patterns of six CYC-like genes from dorsal, lateral, and ventral petals of internal and external florets across capitula of Knautia macedonica (Dipsacaceae). We demonstrate that multiple copies of CYC-like genes are differentially expressed among petal types and between internal and external florets. Across paralogs, there was a general trend toward a reduction in dorsal expression and an increase in ventral expression in internal florets compared to external florets. However, it was in the ventral petals where a statistically significant increase in expression correlates with a less zygomorphic flower. We also show for the first time lateral-specific expression of a CYC-like gene. Additionally, dorsoventral asymmetric expression of a CYC3 paralog indicates that this understudied gene clade is likely also involved in floral symmetry.ConclusionsThese data indicate that the elaboration of bilateral symmetry may be regulated by the dorsoventral gradient of expression, with statistically significant changes in ventral expression correlating with changes in dorsoventral morphological specialization.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-016-0045-7) contains supplementary material, which is available to authorized users.
BackgroundWhile floral symmetry has traditionally been assessed qualitatively, recent advances in geometric morphometrics have opened up new avenues to specifically quantify flower shape and size using robust multivariate statistical methods. In this study, we examine, for the first time, the ability of geometric morphometrics to detect morphological differences in floral dorsoventral asymmetry following virus-induced gene silencing (VIGS). Using Fedia graciliflora Fisch. & Meyer (Valerianaceae) as a model, corolla shape of untreated flowers was compared using canonical variate analysis to knockdown phenotypes of CYCLOIDEA2A (FgCYC2A), ANTHOCYANIDIN SYNTHASE (FgANS), and empty vector controls. ResultsUntreated flowers and all VIGS treatments were morphologically distinct from each other, suggesting that VIGS may cause subtle shifts in floral shape. Knockdowns of FgCYC2A were the most dramatic, affecting the position of dorsal petals in relation to lateral petals, thereby resulting in more actinomorphic-like flowers. Additionally, FgANS knockdowns developed larger flowers with wider corolla tube openings.ConclusionsThese results provide a method to quantify the role that specific genes play in the developmental pathway affecting the dorsoventral axis of symmetry in zygomorphic flowers. Additionally, they suggest that ANS may have an unintended effect on floral size and shape.Electronic supplementary materialThe online version of this article doi: (10.1186/s12870-017-1152-x) contains supplementary material, which is available to authorized users.
We re‐examined the recent study by Palazzesi et al., (2012) published in the Biological Journal of the Linnean Society (107: 67–85), that presented the historical diversification of Geraniales using BEAST analysis of the plastid spacer trnL–F and of the non‐coding nuclear ribosomal internal transcribed spacers (ITS). Their study presented a set of new fossils within the order, generated a chronogram for Geraniales and other rosid orders using fossil‐based priors on five nodes, demonstrated an Eocene radiation of Geraniales (and other rosid orders), and argued for more recent (Pliocene–Pleistocene) and climate‐linked diversification of genera in the five recognized families relative to previous studies. As a result of very young ages for the crown of Geraniales and other rosid orders, unusual relationships of Geraniales to other rosids, and apparent nucleotide substitution saturation of the two gene regions, we conducted a broad series of BEAST analyses that incorporated additional rosid fossil priors, used more accepted rosid ordinal topologies, or altered the placement of one fossil Geraniales prior. Our results indicate that their ages are 20–50% too young owing to a combination of (1) strong nucleotide saturation of the DNA regions starting at 65 Mya, (2) lack of a root (rosid stem) or other rosid ordinal stem fossil‐based priors, (3) the inability of the two DNA regions (with alignment issues) to obtain a monophyletic Geraniales as well as reasonable relationships of Geraniales to other rosid orders, and (4) apparent issues with the nodal placement of a Pelargonium fossil. The Geraniales crown is much older (Campanian of the Cretaceous; 86 Mya), the posterior age distribution on all but two fossil nodes are well older than the priors, the placement of a Pelargonium‐like fossil is more likely at the crown rather than the stem, but their models of diversification within several clades linked to climatic and orogeny appear supported. We discuss a number of the inherent issues of relaxed‐clock dating and outline some ‘best practice’ approaches for such studies. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 29–49.
CYCLOIDEA (CYC) is a TCP transcription factor that has been shown to be involved in specifying dorsal identity in the petals of bilateral flowers. In the plant order Dipsacales, DNA sequencing has provided evidence that multiple, different functional copies of CYC have evolved, most likely via whole genome duplication events in the past. Previous studies of Dipsacales have generated gene trees for the various CYC copies; however, no one has tested if the different copies of CYC are under different selection pressures. Using several programs on the Datamonkey web server, we attempt to determine: (1) whether negative (purifying) selection, neutral evolution, or positive selection are acting on CYC; (2) are the different copies of CYC under different selective pressures; (3) is selection acting on the entire gene, certain amino acids or specific nucleotide sites; and (4) are shifts in selection detected following gene duplication and speciation. Grant Funding Source: Supported by National Science Foundation
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