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Comparative Transcriptome Analyses of Flower Development in Four Species of Achimenes (Gesneriaceae) Wade R Roberts and Roalson BMC Genomics (2017) 18:240 DOI 10.1186/s12864-017-3623-8 RESEARCH ARTICLE Open Access Comparative transcriptome analyses of flower development in four species of Achimenes (Gesneriaceae) Wade R. Roberts1,2* and Eric H. Roalson1,2 Abstract Background: Flowers have an amazingly diverse display of colors and shapes, and these characteristics often vary significantly among closely related species. The evolution of diverse floral form can be thought of as an adaptive response to pollination and reproduction, but it can also be seen through the lens of morphological and developmental constraints. To explore these interactions, we use RNA-seq across species and development to investigate gene expression and sequence evolution as they relate to the evolution of the diverse flowers in a group of Neotropical plants native to Mexico—magic flowers (Achimenes, Gesneriaceae). Results: The assembled transcriptomes contain between 29,000 and 42,000 genes expressed during development. We combine sequence orthology and coexpression clustering with analyses of protein evolution to identify candidate genes for roles in floral form evolution. Over 25% of transcripts captured were distinctive to Achimenes and overrepresented by genes involved in transcription factor activity. Using a model-based clustering approach we find dynamic, temporal patterns of gene expression among species. Selection tests provide evidence of positive selection in several genes with roles in pigment production, flowering time, and morphology. Combining these approaches to explore genes related to flower color and flower shape, we find distinct patterns that correspond to transitions of floral form among Achimenes species. Conclusions: The floral transcriptomes developed from four species of Achimenes provide insight into the mechanisms involved in the evolution of diverse floral form among closely related species with different pollinators. We identified several candidate genes that will serve as an important and useful resource for future research. High conservation of sequence structure, patterns of gene coexpression, and detection of positive selection acting on few genes suggests that large phenotypic differences in floral form may be caused by genetic differences in a small set of genes. Our characterized floral transcriptomes provided here should facilitate further analyses into the genomics of flower development and the mechanisms underlying the evolution of diverse flowers in Achimenes and other Neotropical Gesneriaceae. Keywords: Comparative transcriptomics, Flower evolution, Gesneriaceae, Coexpression clustering, RNA-seq Background the phenotypic diversity of flowers is both visually striking Flowers are a common way that humans connect to na- and evolutionarily intriguing. Flower evolution is often ture and the variety of colors and shapes remains one of thought about from an adaptive perspective with the evo- the most visible and amazing products of evolution. Inno- lution of floral form viewed as a function of reproductive vations in floral form have been proposed as one of the biology or pollination biology [2]. However, developmental primary mechanisms of angiosperm diversification [1] and constraints and morphological potential can also be viewed as a function of floral organogenesis, morphology, * Correspondence: [email protected] and development rather than strictly an adaptive response 1Molecular Plant Sciences Graduate Program, Washington State University, [3]. In recent years, studies of flower morphology in an Pullman, WA 99164-1030, USA 2School of Biological Sciences, Washington State University, Pullman, WA evolutionary and comparative context have been lifted by 99164-4236, USA genetic analyses of developmental pathways underlying © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Roberts and Roalson BMC Genomics (2017) 18:240 Page 2 of 26 flower morphogenesis and biochemistry [4]. However, cettoana, A. erecta, A. misera, and A. patens. This sam- understanding the macroevolutionary consequences of pling strategy allows inter- and intraspecies comparisons flower modification through genetic and microevolution- of gene expression during development and comparisons ary processes remains difficult. The difficulty arises from of sequence structure in order to begin investigating the multitude of possible genetic changes available to evolutionary and developmental mechanisms contribut- produce these phenotypic adaptations. Combining the ing to speciation and diversification. Utilizing high- power of transcriptome sequencing with comparative throughput technologies has allowed researchers in both floral morphology allows for the exploration of the animal [14, 15] and plant [16–18] systems to sequence possible evolutionary genetic mechanisms involved in entire genomes, transcriptomes, and proteomes in order flower development and diversification. to understand fine-scale patterns of genetics and evolu- We provide a first characterization of the floral tran- tion. Our study takes advantage of these genomic scriptomes in four species of magic flowers, Achimenes. approaches and provides resources that will serve as the This small genus of ~26 species is a member of the basis for future studies into flower development, evo- African violet family (Gesneriaceae), a large family distrib- lution, and plant-pollinator interactions. uted in the New World and Old World tropics. The family Comparative transcriptomic studies in plants have seen is renowned for its enormous diversity in habit, desicca- an increasing publication rate in recent years as sequen- tion tolerance, leaf morphology, and, particularly, floral cing technologies keep increasing data output for lower form [5–7]. Flower shape, color, and presentation are cost. Many studies have taken a focused look at compar- hypothesized to be important for diversification and speci- ing developmental stages in a single species across ation events in the family [7–11]. Convergence in floral different tissues [19–21], comparing gene expression in form is found across the family as well as in individual different organs [22, 23], or simply to generate preliminary genera and is likely tied to pollinator preferences and pol- genomic data that will guide more detailed studies linator availability [7, 11]. In Achimenes, floral form [24–27]. Evolutionary questions have also been investigated appears to be quite variable among closely related species using genome-wide expression data in plants, such as the and similar corolla shapes and colors are found among evolution of gene expression patterns [16], parasitism [18], species that occur in different clades [10] (Fig. 1). Multiple self-fertilization [28], or mass flowering [29]. Our study derivations of flower shape, color, and the presence of a aims to bridge the gap between these different areas. We petal spur appear across the genus [10] (Fig. 1). Populations took a developmental approach by sampling several stages of Achimenes are largely concentrated in central Mexico of flower development and an evolutionary approach by south to Costa Rica, with some populations existing in the comparing transcriptome data across multiple species. This Caribbean. General distributions of many closely related evolutionary-developmental approach to comparative tran- species often overlap with many populations found growing scriptomics presents a novel way to investigate the patterns in the same habitat and elevation ranges [12]. Pollinator and processes of flower diversification at the genomic level. studies have been limited with observations recorded for This study provides annotated reference transcriptomes for only four species of Achimenes [13]. The major pol- four species of Achimenes and uses them for analyses of linator observed for each of the four Achimenes sequence orthology, coexpression clustering of genes species corresponds tightly with the hypothesized during development, and selection tests to identify protein pollination syndrome that was identified using combi- sites undergoing positive selection. We also use data from nations of floral traits thought to be important for the transcriptomes to begin investigating the genetics of pollinator attraction, such as color, shape, size, and orien- flower color, particularly the production of anthocya- tation of the open flower [10]. The young age of the genus nin pigments. It is our goal that the resources and (~12 Ma) [7], coupled with a large number of shifts in results provided herein will serve as the basis for flower shape, color, and pollination syndrome [10], makes future studies. This study isamongthefirstexplora- Achimenes an ideal lineage to begin understanding the tions of Neotropical Gesneriaceae flower transcrip- ecological, evolutionary, and molecular forces contributing tomes using large-scale sequencing, and the results to speciation and diversification of floral form. described here may serve to guide further gene Here, we present
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