An expanded evolutionary role for flower symmetry genes

CYCLOIDEA (CYC)-like TCP genes are critical for flower developmental patterning. Exciting recent breakthroughs, including a study by Song et al. published in BMC Evolutionary Biology, demonstrate that CYC-like genes have also had an important role in the evolution of flower form. See research article http://www.biomedcentral.com/1471-2148/9/244 webcite

A CYC–RAD–DIV–DRIF interaction likely pre-dates the origin of floral monosymmetry in Lamiales

Background An outstanding question in evolutionary biology is how genetic interactions defining novel traits evolve. They may evolve either by de novo assembly of previously non-interacting genes or by en bloc co-option of interactions from other functions. We tested these hypotheses in the context of a novel phenotype—Lamiales flower monosymmetry—defined by a developmental program that relies on regulatory interaction among CYCLOIDEA, RADIALIS, DIVARICATA, and DRIF gene products. In Antirrhinum majus (snapdragon), representing Lamiales, we tested whether components of this program likely function beyond their previously known role in petal and stamen development. In Solanum lycopersicum (tomato), representing Solanales which diverged from Lamiales before the origin of Lamiales floral monosymmetry, we additionally tested for regulatory interactions in this program. Results We found that RADIALIS, DIVARICATA, and DRIF are expressed in snapdragon ovaries and developing fruit, similar to their homologs during tomato fruit development. In addition, we found that a tomato CYCLOIDEA ortholog positively regulates a tomato RADIALIS ortholog. Conclusion Our results provide preliminary support to the hypothesis that the developmental program defining floral monosymmetry in Lamiales was co-opted en bloc from a function in carpel development. This expands our understanding of novel trait evolution facilitated by co-option of existing regulatory interactions

Parallel evolution of TCP and B-class genes in Commelinaceae flower bilateral symmetry

<p>Abstract</p> <p>Background</p> <p>Flower bilateral symmetry (zygomorphy) has evolved multiple times independently across angiosperms and is correlated with increased pollinator specialization and speciation rates. Functional and expression analyses in distantly related core eudicots and monocots implicate independent recruitment of class II TCP genes in the evolution of flower bilateral symmetry. Furthermore, available evidence suggests that monocot flower bilateral symmetry might also have evolved through changes in B-class homeotic MADS-box gene function.</p> <p>Methods</p> <p>In order to test the non-exclusive hypotheses that changes in TCP and B-class gene developmental function underlie flower symmetry evolution in the monocot family Commelinaceae, we compared expression patterns of <it>teosinte branched1 </it>(<it>TB1</it>)-like, <it>DEFICIENS </it>(<it>DEF</it>)-like, and <it>GLOBOSA </it>(<it>GLO</it>)-like genes in morphologically distinct bilaterally symmetrical flowers of <it>Commelina communis </it>and <it>Commelina dianthifolia</it>, and radially symmetrical flowers of <it>Tradescantia pallida</it>.</p> <p>Results</p> <p>Expression data demonstrate that <it>TB1</it>-like genes are asymmetrically expressed in tepals of bilaterally symmetrical <it>Commelina</it>, but not radially symmetrical <it>Tradescantia</it>, flowers. Furthermore, <it>DEF</it>-like genes are expressed in showy inner tepals, staminodes and stamens of all three species, but not in the distinct outer tepal-like ventral inner tepals of <it>C. communis</it>.</p> <p>Conclusions</p> <p>Together with other studies, these data suggest parallel recruitment of <it>TB1</it>-like genes in the independent evolution of flower bilateral symmetry at early stages of <it>Commelina </it>flower development, and the later stage homeotic transformation of <it>C. communis </it>inner tepals into outer tepals through the loss of <it>DEF</it>-like gene expression.</p

Parallelism in Flower Evolution and Development

Posted with permission from the Annual Review of Ecology, Evolution, and Systematics, v.51. Copyright by Annual Reviews, http://www.annualreviews.orgFlower evolution is characterized by widespread repetition, with adaptations to pollinator environment evolving in parallel. Recent studies have expanded our understanding of the developmental basis of adaptive floral novelties—petal fusion, bilateral symmetry, heterostyly, and floral dimensions. In this article, we describe patterns of trait evolution and review developmental genetic mechanisms underlying floral novelties. We discuss the diversity of mechanisms for parallel adaptation, the evidence for constraints on these mechanisms, and how constraints help explain observed macroevolutionary patterns. We describe parallel evolution resulting from similarities at multiple hierarchical levels—genetic, developmental, morphological, functional—which indicate general principles in floral evolution, including the central role of hormone signaling. An emerging pattern is mutational bias that may contribute to rapid patterns of parallel evolution, especially if the derived trait can result from simple degenerative mutations. We argue that such mutational bias may be less likely to govern the evolution of novelties patterned by complex developmental pathways

Reduce, reuse, and recycle: Developmental evolution of trait diversification

This is the publisher's version, also available electronically from http://www.amjbot.org.A major focus of evolutionary developmental (evo-devo) studies is to determine the genetic basis of variation in organismal form and function, both of which are fundamental to biological diversification. Pioneering work on metazoan and flowering plant systems has revealed conserved sets of genes that underlie the bauplan of organisms derived from a common ancestor. However, the extent to which variation in the developmental genetic toolkit mirrors variation at the phenotypic level is an active area of research. Here we explore evidence from the angiosperm evo-devo literature supporting the frugal use of genes and genetic pathways in the evolution of developmental patterning. In particular, these examples highlight the importance of genetic pleiotropy in different developmental modules, thus reducing the number of genes required in growth and development, and the reuse of particular genes in the parallel evolution of ecologically important traits

Parental experience modifies the Mimulus methylome

This work is licensed under a Creative Commons Attribution 4.0 International License.Background Transgenerational plasticity occurs when the environmental experience of an organism modifies the growth and development of its progeny. Leaf damage in Mimulus guttatus exhibits transgenerational plasticity mediated through differential expression of hundreds of genes. The epigenetic mechanisms that facilitate this response have yet to be described. Results We performed whole genome bisulfite sequencing in the progeny of genetically identical damaged and control plants and developed a pipeline to compare differences in the mean and variance of methylation between treatment groups. We find that parental damage increases the variability of CG and CHG methylation among progeny, but does not alter the overall mean methylation. Instead it has positive effects in some regions and negative in others. We find 3,396 CHH, 203 CG, and 54 CHG Differentially Methylated Regions (DMRs) ranging from tens to thousands of base pairs scattered across the genome. CHG and CHH DMRs tended to overlap with transposable elements. CG DMRs tended to overlap with gene coding regions, many of which were previously found to be differentially expressed. Conclusions Genome-wide increases in methylome variation suggest that parental conditions can increase epigenetic diversity in response to stress. Additionally, the potential association between CG DMRs and differentially expressed genes supports the hypothesis that differential methylation is a mechanistic component of transgenerational plasticity in M. guttatus.University of Kansas Botany EndowmentNSF IOS-0951254Kansas-INBRE P20-GM10341

Novel Traits, Flower Symmetry, and Transcriptional Autoregulation: New Hypotheses From Bioinformatic and Experimental Data

A common feature in developmental networks is the autoregulation of transcription factors which, in turn, positively or negatively regulate additional genes critical for developmental patterning. When a transcription factor regulates its own expression by binding to cis-regulatory sites in its gene, the regulation is direct transcriptional autoregulation (DTA). Indirect transcriptional autoregulation (ITA) involves regulation by proteins expressed downstream of the target transcription factor. We review evidence for a hypothesized role of DTA in the evolution and development of novel flowering plant phenotypes. We additionally provide new bioinformatic and experimental analyses that support a role for transcriptional autoregulation in the evolution of flower symmetry. We find that 5′ upstream non-coding regions are significantly enriched for predicted autoregulatory sites in Lamiales CYCLOIDEA genes—an upstream regulator of flower monosymmetry. This suggests a possible correlation between autoregulation of CYCLOIDEA and the origin of monosymmetric flowers near the base of Lamiales, a pattern that may be correlated with independently derived monosymmetry across eudicot lineages. We find additional evidence for transcriptional autoregulation in the flower symmetry program, and report that Antirrhinum DRIF2 may undergo ITA. In light of existing data and new data presented here, we hypothesize how cis-acting autoregulatory sites originate, and find evidence that such sites (and DTA) can arise subsequent to the evolution of a novel phenotype

Paralogous SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes differentially regulate leaf initiation and reproductive phase change in petunia

Duplicated petunia clade-VISPLgenes differentially promote the timing of inflorescence and flower development, and leaf initiation rate. The timing of plant reproduction relative to favorable environmental conditions is a critical component of plant fitness, and is often associated with variation in plant architecture and habit. Recent studies have shown that overexpression of the microRNA miR156 in distantly related annual species results in plants with perennial characteristics, including late flowering, weak apical dominance, and abundant leaf production. These phenotypes are largely mediated through the negative regulation of a subset of genes belonging to the SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) family of transcription factors. In order to determine how and to what extent paralogous SPL genes have partitioned their roles in plant growth and development, we functionally characterized petunia clade-VI SPL genes under different environmental conditions. Our results demonstrate that PhSBP1and PhSBP2 differentially promote discrete stages of the reproductive transition, and that PhSBP1, and possibly PhCNR, accelerates leaf initiation rate. In contrast to the closest homologs in annual Arabidopsis thaliana and Mimulus guttatus, PhSBP1 and PhSBP2 transcription is not mediated by the gibberellic acid pathway, but is positively correlated with photoperiod and developmental age. The developmental functions of clade-VI SPL genes have, thus, evolved following both gene duplication and speciation within the core eudicots, likely through differential regulation and incomplete sub-functionalization

DNA methylation and gene expression in Mimulus guttatus

Background The presence of methyl groups on cytosine nucleotides across an organism’s genome (methylation) is a major regulator of genome stability, crossing over, and gene regulation. The capacity for DNA methylation to be altered by environmental conditions, and potentially passed between generations, makes it a prime candidate for transgenerational epigenetic inheritance. Here we conduct the first analysis of the Mimulus guttatus methylome, with a focus on the relationship between DNA methylation and gene expression. Results We present a whole genome methylome for the inbred line Iron Mountain 62 (IM62). DNA methylation varies across chromosomes, genomic regions, and genes. We develop a model that predicts gene expression based on DNA methylation (R2 = 0.2). Post hoc analysis of this model confirms prior relationships, and identifies novel relationships between methylation and gene expression. Additionally, we find that DNA methylation is significantly depleted near gene transcriptional start sites, which may explain the recently discovered elevated rate of recombination in these same regions. Conclusions The establishment here of a reference methylome will be a useful resource for the continued advancement of M. guttatus as a model system. Using a model-based approach, we demonstrate that methylation patterns are an important predictor of variation in gene expression. This model provides a novel approach for differential methylation analysis that generates distinct and testable hypotheses regarding gene expression

Non-equilibrium dynamics and floral trait interactions shape extant angiosperm diversity.

Why are some traits and trait combinations exceptionally common across the tree of life, whereas others are vanishingly rare? The distribution of trait diversity across a clade at any time depends on the ancestral state of the clade, the rate at which new phenotypes evolve, the differences in speciation and extinction rates across lineages, and whether an equilibrium has been reached. Here we examine the role of transition rates, differential diversification (speciation minus extinction) and non-equilibrium dynamics on the evolutionary history of angiosperms, a clade well known for the abundance of some trait combinations and the rarity of others. Our analysis reveals that three character states (corolla present, bilateral symmetry, reduced stamen number) act synergistically as a key innovation, doubling diversification rates for lineages in which this combination occurs. However, this combination is currently less common than predicted at equilibrium because the individual characters evolve infrequently. Simulations suggest that angiosperms will remain far from the equilibrium frequencies of character states well into the future. Such non-equilibrium dynamics may be common when major innovations evolve rarely, allowing lineages with ancestral forms to persist, and even outnumber those with diversification-enhancing states, for tens of millions of years