Identification of Conserved Aquilegia Coerulea MicroRNAs and Their Targets

Aquilegia is an emerging model organism that is phylogenetically intermediate between the core eudicot and monocot models, Arabidopsis and Oryza. In this study, we have used a comparative genomics approach to identify 45 Aquilegia microRNAs that comprise 20 separate plant microRNA families. We have predicted 84 targets of these newly identified Aquilegia microRNAs including transcription factors and loci involved in metabolism, stress responses, transport, and auxin signaling. microRNA families from 16 plant species and the newly identified microRNAs from Aquilegia were analyzed in a phylogenetic context revealing 40 distantly conserved microRNA families. In addition to these highly conserved plant microRNA families, several families with disjointed phylogenetic distribution were identified. This study provides a phylogenetically important dataset for plant microRNA evolution studies. The current study is the first to identify miRNAs in a lower eudicot in which comprehensive genomic resources are becoming available.Organismic and Evolutionary Biolog

Evolution of Spur-Length Diversity in Aquilegia Petals Is Achieved Solely Through Cell-Shape Anisotropy

The role of petal spurs and specialized pollinator interactions has been studied since Darwin. Aquilegia petal spurs exhibit striking size and shape diversity, correlated with specialized pollinators ranging from bees to hawkmoths in a textbook example of adaptive radiation. Despite the evolutionary significance of spur length, remarkably little is known about Aquilegia spur morphogenesis and its evolution. Using experimental measurements, both at tissue and cellular levels, combined with numerical modelling, we have investigated the relative roles of cell divisions and cell shape in determining the morphology of the Aquilegia petal spur. Contrary to decades-old hypotheses implicating a discrete meristematic zone as the driver of spur growth, we find that Aquilegia petal spurs develop via anisotropic cell expansion. Furthermore, changes in cell anisotropy account for 99 per cent of the spur-length variation in the genus, suggesting that the true evolutionary innovation underlying the rapid radiation of Aquilegia was the mechanism of tuning cell shape.Engineering and Applied SciencesOrganismic and Evolutionary Biolog

Origin and evolution of the octoploid strawberry genome.

Cultivated strawberry emerged from the hybridization of two wild octoploid species, both descendants from the merger of four diploid progenitor species into a single nucleus more than 1 million years ago. Here we report a near-complete chromosome-scale assembly for cultivated octoploid strawberry (Fragaria × ananassa) and uncovered the origin and evolutionary processes that shaped this complex allopolyploid. We identified the extant relatives of each diploid progenitor species and provide support for the North American origin of octoploid strawberry. We examined the dynamics among the four subgenomes in octoploid strawberry and uncovered the presence of a single dominant subgenome with significantly greater gene content, gene expression abundance, and biased exchanges between homoeologous chromosomes, as compared with the other subgenomes. Pathway analysis showed that certain metabolomic and disease-resistance traits are largely controlled by the dominant subgenome. These findings and the reference genome should serve as a powerful platform for future evolutionary studies and enable molecular breeding in strawberry

The case for the continued use of the genus name Mimulus for all monkeyflowers

The genus Mimulus is a well-studied group of plant species, which has for decades allowed researchers to address a wide array of fundamental questions in biology (Wu & al. 2008; Twyford & al. 2015). Linnaeus named the type species of Mimulus (ringens L.), while Darwin (1876) used Mimulus (luteus L.) to answer key research questions. The incredible phenotypic diversity of this group has made it the focus of ecological and evolutionary study since the mid-20th century, initiated by the influential work of Clausen, Keck, and Hiesey as well as their students and collaborators (Clausen & Hiesey 1958; Hiesey & al. 1971, Vickery 1952, 1978). Research has continued on this group of diverse taxa throughout the 20th and into the 21st century (Bradshaw & al. 1995; Schemske & Bradshaw 1999; Wu & al. 2008; Twyford & al. 2015; Yuan 2019), and Mimulus guttatus was one of the first non-model plants to be selected for full genome sequencing (Hellsten & al. 2013). Mimulus has played a key role in advancing our general understanding of the evolution of pollinator shifts (Bradshaw & Schemske 2003; Cooley & al. 2011; Byers & al. 2014), adaptation (Lowry & Willis 2010; Kooyers & al. 2015; Peterson & al. 2016; Ferris & Willis 2018; Troth & al. 2018), speciation (Ramsey & al. 2003; Wright & al. 2013; Sobel & Streisfeld 2015; Zuellig & Sweigart 2018), meiotic drive (Fishman & Saunders 2008), polyploidy (Vallejo-Marín 2012; Vallejo-Marín & al. 2015), range limits (Angert 2009; Sexton et al. 2011; Grossenbacher & al. 2014; Sheth & Angert 2014), circadian rhythms (Greenham & al. 2017), genetic recombination (Hellsten & al. 2013), mating systems (Fenster & Ritland 1994; Dudash & Carr 1998; Brandvain & al. 2014) and developmental biology (Moody & al. 1999; Baker & al. 2011, 2012; Yuan 2019). This combination of a rich history of study coupled with sustained modern research activity is unparalleled among angiosperms. Across many interested parties, the name Mimulus therefore takes on tremendous biological significance and is recognizable not only by botanists, but also by zoologists, horticulturalists, naturalists, and members of the biomedical community. Names associated with a taxonomic group of this prominence should have substantial inertia, and disruptive name changes should be avoided. As members of the Mimulus community, we advocate retaining the genus name Mimulus to describe all monkeyflowers. This is despite recent nomenclature changes that have led to a renaming of most monkeyflower species to other genera.Additional co-authors: Jannice Friedman, Dena L Grossenbacher, Liza M Holeski, Christopher T Ivey, Kathleen M Kay, Vanessa A Koelling, Nicholas J Kooyers, Courtney J Murren, Christopher D Muir, Thomas C Nelson, Megan L Peterson, Joshua R Puzey, Michael C Rotter, Jeffrey R Seemann, Jason P Sexton, Seema N Sheth, Matthew A Streisfeld, Andrea L Sweigart, Alex D Twyford, John H Willis, Kevin M Wright, Carrie A Wu, Yao-Wu Yua

Plant MicroRNA Evolution and Mechanisms of Shape Change in Plants

Plant microRNAs have been shown to have important roles in regulating diverse processes ranging from reproductive development to stress response. In the first two chapters, I focus on miRNA diversity in Aquilegia studying both anciently evolved broadly conserved and rapidly evolving species specific miRNAs. In chapter one, I utilize Aquilegia's critical phylogenetic position between the well developed models Arabidopsis thaliana and Oryza sativa to study the evolution of ancient miRNAs across the angiosperms. In chapter two, I utilize smallRNA high-throughput sequencing to annotate Aquilegia specific miRNAs and, in the process, uncover the novel regulation of a floral homeotic gene by an Aquilegia-specific miRNA. In chapter three, I look at the tissue specific development of miRNA regulation in the bioenergetically relevant model organism Populus trichocarpa. High-throughput smallRNA sequencing from four diverse tissue sets including leaves, xylem, mechanically treated xylem, and pooled vegetative and reproductive tissues were analyzed, revealing a total of 155 previously unannotated miRNAs, most of which are P. trichocarpa specific. Expanding on my work with the petal identity pathway, I turned a broader analysis of Aquilegia petal spurs. Petal spurs are the distinguishing characteristic of Aquilegia and are argued to be a key innovation in the adaptive radiation of the genus. In the fourth chapter, I explore the cellular basis of extreme spur length diversity in the genus and find that a single parameter, cell shape, can explain this morphological range. Next, I seek to describe the cellular patterns that give rise to a spur primoridia from an initially flat laminar petal and find that spur initiation is characterized by concentrated, prolonged, and oriented cell divisions. Inspired by this quantitative analysis of growth, chapter five looks at the mechanisms of shape change in cucumber tendrils. I find that anisotropic contraction of a multi-layered gelatinous fiber ribbon explains coiling in cucumbers. Surprisingly, we discover that tendrils display twistless-overwinding when pulled and exhibit an unforeseen force-extension response as a result. These results provide the design basis for twistless springs with tunable mechanical responses and serve as a clear example of how the biological systems can inspire applied mechanical designs

The causes and consequences of subgenome dominance in hybrids and recent polyploids

Contents Summary 87 I. Introduction 87 II. Evolution in action: subgenome dominance within newly formed hybrids and polyploids 88 III. Summary and future directions 90 Acknowledgements 92 References 92 SUMMARY: The merger of divergent genomes, via hybridization or allopolyploidization, frequently results in a 'genomic shock' that induces a series of rapid genetic and epigenetic modifications as a result of conflicts between parental genomes. This conflict among the subgenomes routinely leads one subgenome to become dominant over the other subgenome(s), resulting in subgenome biases in gene content and expression. Recent advances in methods to analyze hybrid and polyploid genomes with comparisons to extant parental progenitors have allowed for major strides in understanding the mechanistic basis for subgenome dominance. In particular, our understanding of the role that homoeologous exchange might play in subgenome dominance and genome evolution is quickly growing. Here we describe recent discoveries uncovering the underlying mechanisms and provide a framework to predict subgenome dominance in hybrids and allopolyploids with far-reaching implications for agricultural, ecological, and evolutionary research

Phylogenetic Analyses (trees, alignments, filtered regions)

This zipped directory contains the phylogenetic trees, sequence alignments, and filtered regions

Data from: Strongly asymmetric hybridization barriers shape the origin of a new polyploid species and its hybrid ancestor

PREMISE OF THE STUDY: Hybridization between diploids and tetraploids can lead to new allopolyploid species, often via a triploid intermediate. Viable triploids are often produced asymmetrically, with greater success observed for “maternal-excess” crosses where the mother has a higher ploidy than the father. Here we investigated the evolutionary origins of Mimulus peregrinus, an allohexaploid recently derived from the triploid M. ×robertsii, to determine whether reproductive asymmetry has shaped the formation of this new species. METHODS: We used reciprocal crosses between the diploid (M. guttatus) and tetraploid (M. luteus) progenitors to determine the viability of triploid M. ×robertsii hybrids resulting from paternal- vs. maternal-excess crosses. To investigate whether experimental results predict patterns seen in the field, we performed parentage analyses comparing natural populations of M. peregrinus to its diploid, tetraploid, and triploid progenitors. Organellar sequences obtained from pre-existing genomic data, supplemented with additional genotyping was used to establish the maternal ancestry of multiple M. peregrinus and M. ×robertsii populations. KEY RESULTS: We found strong evidence for asymmetric origins of M. peregrinus, but opposite to the common pattern, with paternal-excess crosses significantly more successful than maternal-excess crosses. These results successfully predicted hybrid formation in nature: 111 of 114 M. ×robertsii individuals, and 27 of 27 M. peregrinus, had an M. guttatus maternal haplotype. CONCLUSION: This study, which includes the first Mimulus chloroplast genome assembly, demonstrates the utility of parentage analysis through genome skimming. We highlight the benefits of complementing genomic analyses with experimental approaches to understand asymmetry in allopolyploid speciation

Data from: Subgenome dominance in an interspecific hybrid, synthetic allopolyploid, and a 140-year-old naturally established neo-allopolyploid monkeyflower

Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally more dominant - having both retained more genes and being more highly expressed - a phenomenon termed subgenome dominance. The genomic features that determine how quickly and which subgenome dominates within a newly formed polyploid remain poorly understood. To investigate the rate of subgenome dominance emergence, we examined gene expression, gene methylation, and transposable element (TE) methylation in a natural, less than 140 year old allopolyploid (Mimulus peregrinus), a resynthesized inter-species triploid hybrid (M. robertsii), a resynthesized allopolyploid (M. peregrinus), and diploid progenitors (M. guttatus and M. luteus). We show that subgenome expression dominance occurs instantly following the hybridization of two divergent genomes and significantly increases over generations. Additionally, CHH methylation levels are significantly reduced in regions near genes and within TEs in the first generation hybrid, intermediate in the resynthesized allopolyploid, and are repatterned differently between the dominant and recessive subgenomes in the natural allopolyploid. In addition, subgenome differences in levels of TE methylation mirror the increase in expression bias observed over the generations following hybridization. These findings provide important insights into genomic and epigenomic shock that occurs following hybridization and polyploid events

Data from: Subgenome dominance in an interspecific hybrid, synthetic allopolyploid, and a 140-year-old naturally established neo-allopolyploid monkeyflower

Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally more dominant - having both retained more genes and being more highly expressed - a phenomenon termed subgenome dominance. The genomic features that determine how quickly and which subgenome dominates within a newly formed polyploid remain poorly understood. To investigate the rate of subgenome dominance emergence, we examined gene expression, gene methylation, and transposable element (TE) methylation in a natural, less than 140 year old allopolyploid (Mimulus peregrinus), a resynthesized inter-species triploid hybrid (M. robertsii), a resynthesized allopolyploid (M. peregrinus), and diploid progenitors (M. guttatus and M. luteus). We show that subgenome expression dominance occurs instantly following the hybridization of two divergent genomes and significantly increases over generations. Additionally, CHH methylation levels are significantly reduced in regions near genes and within TEs in the first generation hybrid, intermediate in the resynthesized allopolyploid, and are repatterned differently between the dominant and recessive subgenomes in the natural allopolyploid. In addition, subgenome differences in levels of TE methylation mirror the increase in expression bias observed over the generations following hybridization. These findings provide important insights into genomic and epigenomic shock that occurs following hybridization and polyploid events