A cornucopia of diversity—Ranunculales as a model lineage
Abstract
The Ranunculales are a hyperdiverse lineage in many aspects of their phenotype, including growth habit, floral and leaf morphology, reproductive mode, and specialized metabolism. Many Ranunculales species, such as opium poppy and goldenseal, have a high medicinal value. In addition, the order includes a large number of commercially important ornamental plants, such as columbines and larkspurs. The phylogenetic position of the order with respect to monocots andcore eudicots and the diversity within this lineage make the Ranunculales an excellent group for studying evolutionary processes by comparative studies. Lately, the phylogeny of Ranunculales was revised, and genetic and were developed for many species, allowing comparative analyses at the molecular scale. Here, we review the literature on the resources for genetic manipulation and genome sequencing, the recent phylogeny reconstruction of this order, and its fossil record. Further, we explain their habitat range and delve into the diversity in their floral morphology,focusing on perianth organ identity, floral symmetry, occurrences of spurs and nectaries, sexual and pollination systems, and fruit and dehiscence types. The Ranunculales order offers a wealth of opportunities for scientific exploration across various disciplines and scales, to gain novel insights into plant biology for researchers and plant enthusiasts alike.
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Copyedited by: OUPCopyedited by: OUP Journal of Experimental Botany, Vol. 75, No. 7 pp. 1800–1822, 2024 https://doi.org/10.1093/jxb/erad492 Advance Access Publication 18 December 2023 © The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/ by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial reuse, please contact [email protected] FLOWERING NEWSLETTER REVIEW A cornucopia of diversity—Ranunculales as a model lineage The RanOmics group, Annette Becker1,*,, Julien B. Bachelier2,, Laetitia Carrive3,, Natalia Conde e Silva4, Catherine Damerval4,, Cédric Del Rio5,, Yves Deveaux4,, Verónica S. Di Stilio6,, Yan Gong7,, Florian Jabbour8,, Elena M. Kramer7,, Sophie Nadot9,, Natalia Pabón-Mora10,, and Wei Wang11, 1 Plant Development Group, Institute of Botany, Justus-Liebig-University, Giessen, Germany 2 Institute of Biology/Dahlem Centre of Plant Sciences, Freie Universität Berlin, D-14195 Berlin, Germany 3 Université de Rennes, UMR CNRS 6553, Ecosystèmes-Biodiversité-Evolution, Campus de Beaulieu, 35042 Rennes cedex, France 4 Université Paris-Saclay, INRAE, CNRS, AgroParisTech, Génétique Quantitative et Evolution-Le Moulon, 91190 Gif-sur-Yvette, France 5 CR2P - Centre de Recherche en Paléontologie - Paris, MNHN - Sorbonne Université - CNRS, 43 Rue Buffon, 75005 Paris, France 6 Department of Biology, University of Washington, Seattle, WA 98195-1800, USA 7 Department of Organismic and Evolutionary Biology, Harvard University, MA, 02138, USA 8 Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum national d’Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, 57 rue Cuvier, CP39, Paris, 75005, France 9 Université Paris-Saclay, CNRS, AgroParisTech, Ecologie, Systématique et Evolution, Gif-sur-Yvette, France 10 Instituto de Biología, Universidad de Antioquia, Medellín, 050010, Colombia 11 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093 China and University of Chinese Academy of Sciences, Beijing, 100049 China * Correspondence: [email protected] Received 15 September 2023; Editorial decision 29 November 2023; Accepted 11 December 2023 Editor: Rainer Melzer, University College Dublin, Ireland Abstract The Ranunculales are a hyperdiverse lineage in many aspects of their phenotype, including growth habit, floral and leaf morphology, reproductive mode, and specialized metabolism. Many Ranunculales species, such as opium poppy and goldenseal, have a high medicinal value. In addition, the order includes a large number of commercially important ornamental plants, such as columbines and larkspurs. The phylogenetic position of the order with respect to monocots and core eudicots and the diversity within this lineage make the Ranunculales an excellent group for studying evolutionary processes by comparative studies. Lately, the phylogeny of Ranunculales was revised, and genetic and genomic resources were developed for many species, allowing comparative analyses at the molecular scale. Here, we review the literature on the resources for genetic manipulation and genome sequencing, the recent phylogeny reconstruction of this order, and its fossil record. Further, we explain their habitat range and delve into the diversity in their floral morphology, focusing on perianth organ identity, floral symmetry, occurrences of spurs and nectaries, sexual and pollination systems, and fruit and dehiscence types. The Ranunculales order offers a wealth of opportunities for scientific exploration across various disciplines and scales, to gain novel insights into plant biology for researchers and plant enthusiasts alike. Keywords: Ancestral states, carpels, distribution, fossils, fruits, genomic resources, nectaries, phyllotaxy, phylogeny, sexual systems, spurs, symmetry. Downloaded from https://academic.oup.com/jxb/article/75/7/1800/7477764 by guest on 23 October 2025
Copyedited by: OUPCopyedited by: OUP Ranunculales model lineage | 1801 Introduction Ranunculales are the sister order to all other eudicots and have diverged before the core eudicots, which include approximately three-quarters of all angiosperms species (The Angiosperm Phylogeny Group, 2016). Studying Ranunculales can thus provide clues to the core eudicot’s ancestral states in terms of morphology and genetics. The order Ranunculales encompasses >4500 species and is composed of seven families: Ranunculaceae, Berberidaceae, Menispermaceae, Lardizabalaceae, Circeasteraceae, Papaveraceae, and Eupteleaceae (Fig. 1; The Angiosperm Phylogeny Group, 2016). They are remarkably diverse in terms of floral and fruit form, life history traits, leaf shape, growth shape, and their secondary metabolite composition. The flowers of Ranunculales are not only unusually diverse in their morphology, they are also unique in concentrating a variety of evolutionary transitions, such as changes in merism (number of floral organs), in phyllotaxy (whorled versus spiral) potentially leading to the emergence of organ fusion (in reproductive organs and perianth), and in the origin of novel organs. These transitions are only rarely observed in monocot or core eudicot model lineages. Further, Ranunculales exhibit a suite of homoplasious characters (shared character states that did not arise from a direct common ancestor, but independently via convergent evolution) such as transitions between sexual systems and pollination modes in closely related taxa, petal loss, spur formation, or transition to zygomorphy (Endress, 1995; Soza et al., 2012; Damerval and Becker, 2017; Becker et al., 2023). Homoplasies and the emergence of novel organs provide premier opportunities to study the molecular and genetic mechanisms involved in the origin of these special traits using species within Ranunculales as case studies. Aside from their morphological diversity, Ranunculales produce a multitude of secondary metabolites, many of them of pharmaceutical importance. Consequently, Ranunculales species have been used in traditional medicine since at least the early civilizations. Some species, such as Nigella sativa, were already mentioned in writing by, for example, Ayurveda, Siddha, Fig 1. Simplified phylogeny of Ranunculales based on Wang etal. (2009), Ortiz etal. (2016), and Peng etal. (2023). Species for which major genomic resources are or will become available in the near future are next to their respective branches. Representative photos of Ranunculales flowers: (A) Aquilegia coerulea, (B) Thalictrum thalictroides, (C) Nigella damascena, (D) Staphisagria picta (Ranunculaceae), (E) Epimedium grandiflorum (Berberidaceae), (F) Pteridophyllum racemosum, (G) Capnoides sempervirens, (H) Eschscholzia californica, (I) Macleaya cordata, (J) Papaver somniferum (Papaveraceae). (Photo credit: A, D–G, H, J, Becker lab; B, Di Stilio lab; C, F, Jabbour; I, N, Pabón Mora.) Downloaded from https://academic.oup.com/jxb/article/75/7/1800/7477764 by guest on 23 October 2025
Copyedited by: OUPCopyedited by: OUP 1802 | Becker et al. Unani, Greek–Roman, Malay, Tibb-e-Nabwi, and Jewish civilizations (Heiss and Oeggl, 2005; Dabeer etal., 2022). The use of opium poppy (Papaver somniferum) as a narcotic drug dates even back to the Neolithic (Guerra-Doce, 2015; Yang etal., 2021). New World indigenous cultures used Ranunculales; for example, Navajos used Thalictrum fendleri tea during ceremonial war dance rites (Elmore, 1943) and Pomo women used Eschscholzia californica during infant weaning (Barrett, 1952). Ranunculales are a rich source of economically important phytochemicals, such as alkaloids, diterpenes, triterpenes, isoquinoline alkaloids, and cardiac as well as cyanogenic glycosides (Hao etal., 2015). These compounds contribute to a vast array of medicinal uses for different Ranunculales species, for example in ulcer treatment, and as antimicrobe and anti-inflammatory agents (Hao etal., 2015). Papaveraceae are notoriously known for their secondary metabolite diversity, and many of their compounds are essential pharmaceuticals of high economic value, including morphine, codeine, protopine, isocorydine, or berberine. Benzisoquinoline alkaloids (BIAs) in particular are well known for their analgesic, antitussive, antimicrobial, anticancer, and anti-inflammatory effect (Li etal., 2020; Avci etal., 2021; Becker etal., 2023). Of special pharmaceutical importance are morphine and codeine used as analgesics, the anticancer drug noscapine, and antibacterial compounds such as sanguinarine (Hagel and Facchini, 2013). Members of the other Ranunculales families synthesize unique and overlapping subsets of secondary metabolites (Hao etal., 2015). Consequently, a wide array of species is used as herbal extracts, even nowadays, for example in Chinese traditional medicine (Hao etal., 2015, 2017). An informative phylogenetic position, combined with pharmacological relevance and stunning floral morphological diversity, has led to a strong research interest in the Ranunculales, resulting in the development of an array of genetic tools to aid in the investigation of gene function and regulation (Di Stilio, 2011; Becker etal., 2023). The powerful combination of genetic studies, comparative morphology, and secondary metabolite profiling will further enable the reconstruction of ancestral traits before the major core eudicot radiation. In this review, we present an update on the phylogeny, fossil records, and ecology of Ranunculales, before adressing recent findings concerning the genetic origin, diversity, and evolution of floral and fruit traits. We also recapitulate the available omics resources and functional tools, and introduce the RanOmics project, aiming at selecting phylogenetically informative species to unravel the evolution of ecologically and economically important traits. Genetic resources and functional tools for Ranunculales In the ‘omics’ era, several genetic resources have been established for Ranunculales, mostly for mining genes related to secondary metabolite biosynthesis and regulation. The number of high-quality Ranunculales genomes, starting with the first sequenced genome from Macleaya cordata (Liu etal., 2017), has increased enormously in the past few years, allowing for comparative genome analysis (Fig. 1; Table 1). However, the suitability criteria for high quality reference genomes are unclear, hence we define them here as follows: the rate of Benchmarking Universal Single-Copy Orthologs (BUSCO; Manni et al., 2021) matches should be >95%. Table 1 shows that only two Ranunculales genomes match this criterion, these are P. somniferum (opium poppy) and Corydalis tomentella (Guo et al., 2018; Xu etal., 2022). Genomes with lower BUSCO values are available for Thalictrum thalictroides, Coptis chinensis, Aquilegia coerulea, and Aquilegia oxysepala (Ranunculaceae), Kingdonia uniflora (Circeasteraceae), Akebia trifoliata (Lardizabalaceae), Epimedium pubescens (Berberidaceae), Eschscholzia californica, Corydalis tomentella, Papaver somniferum, Papaver rhoeas, Papaver setigerum, and Macleaya chordata (Papaveraceae) (Liu etal., 2017, 2021; Filiault etal., 2018; Hori etal., 2018; Sun etal., 2020; Xie etal., 2020; Arias etal., 2021; Chen etal., 2021; Huang etal., 2021; Yang etal., 2021; Shen etal., 2022). The available genomes already provide sufficient data for the inference of whole-genome duplications (WGDs) within the Ranunculales. When the genomes of P. somniferum, M. cordata, A. coerulea, and C. chinensis were analyzed in combination, one WGD was found to have probably occurred in the lineage leading to C. chinensis and A. coerulea, and another one in the lineage leading to P. somniferum and M. cordata (Liu etal., 2021). An additional WGD was identified in the lineage leading to P. somniferum and P. setigerum, which is not shared by P. rhoeas and M. cordata. Moreover, the P. setigerum genome shows an additional WGD (Yang etal., 2021), most probably contributing to its large genome size, which is almost double that of the closely related P. somniferum. These recent comparative genome studies suggest that the genome duplication history of Ranunculales is most likely to be as complex as those of the core eudicots, considering that the number of sequenced Ranunculales genomes is still relatively small. Recently, the molecular evolution of morphine biosynthesis in the Papaveraceae was unraveled by comparative genomics: the final morphine biosynthesis steps, which require the STORR gene modules, was found to be <18 million years old (Li etal., 2020). The STORR gene, coding for the key enzyme converting morphinans to morphine, originated from a translational fusion of a cytochrome P450 and an oxidoreductase enzyme that occurred after the split of P. setigerum and P. somniferum from P. rhoeas and was then duplicated in the P. setigerumspecific WGD (Li etal., 2020; Yang etal., 2021). The 1KP project (One Thousand Plant Transcriptomes Initiative, 2019) has provided transcriptomic data for a single or a few tissues of these Ranunculales species: the Lardizabalaceae A. trifoliata; the Menispermaceae Cocculus laurifolius; the Eupteleaceae Euptelea pleiosperma; the Berberidaceae Nandina domestica and Podophyllum peltatum; the Ranunculaceae Anemone hupehensis, Anemone pulsatilla, Cimicifuga racemosa, Hydrastis canadensis, and Downloaded from https://academic.oup.com/jxb/article/75/7/1800/7477764 by guest on 23 October 2025
Copyedited by: OUPCopyedited by: OUP Ranunculales model lineage | 1803 Table 1. Genomic resources for RanOmics Ranunculales species Species Genome available BUSCOaCell/callus culture system Cell culture transformation system Stable transformation Virus-inducedgene silencing Spontaneous mutants Papaveraceae Eschscholzia californicab Hori etal. (2018) Not given Hauschild etal. (1998) Fujii etal. (2007) Park and Facchini, (2000b); Lotz etal. (2022) Wege etal. (2007) Lange etal., 2013; Wakelin etal. (2003); Barrell etal. (2010); Pollack etal. (2019); Conner and Barrell (2014) Papaver somniferumb Guo etal. (2018) 95.3 Eilert etal. (1985) Belny etal. (1997) Park and Facchini, (2000a); Chitty etal. (2003) Hilemann etal. (2005) Singh etal. (2017); Pathak etal. (2013); Dhawan etal. (2007); Belyaeva and Nevkrytaya (1979); Prajapati etal. (2001); Singh etal. (2014) Macleaya cordata Liu etal. (2017) 90.4 Franke and Böhm (1982) No Huang etal. (2017) No Papaver rhoeas Yang etal. (2021) 92.8 No No No No O’Donnell etal. (1993); Foote etal., (1994) Papaver setigerum Yang etal. (2021) 94.5 No No No no Corydalis tomentella Xu etal. (2022) 97.67 Holländer-Czytko etal. (1988) (Corydalis sempervirens) No No No Capnoides sempervirensb No No No Hidalgo etal. (2012) Pteridophyllum racemosumb No No No No Ranunculaceae Coptis chinensis Chen etal. (2021) 91.5 No No No No Aquilegia coeruleabFiliaut etal. (2018) Not given No No No Gould and Kramer (2007) Cabin etal. (2022) Aquilegia oxysepala Xie etal. (2020) 93.2 No No No No Thalictrum thalictroidesb Arias etal. (2021) 84.5 Smolko and Peretti (1994) Samanani etal. (2002) (Thalictrum flavum) No Di Stilio etal. (2010) Martinez-Gómez etal. (2021); Galimba etal. (2012) Nigella damascenab Klimek-Chodacka etal. (2020) No Wang etal. (2015) Goncalvez etal. (2013); Jabbour etal. (2021); Conde e Silva etal. (2023); Greyson and Raman (1975) Staphisagria pictab No No No No Hydrastis canadensisb No No No No Cicaeasteraceae Downloaded from https://academic.oup.com/jxb/article/75/7/1800/7477764 by guest on 23 October 2025
Copyedited by: OUPCopyedited by: OUP 1804 | Becker et al. T. thalictroides; and the Papaveraceae Argemone mexicana, Capnoides sempervirens, Ceratocapnos vesicaria, Chelidonium majus, Corydalis linstowiana, E. californica, Hypecoum procumbens, Papaver bracteatum, P. rhoeas, P. setigerum, P. somniferum, and Sanguinaria canadensis. Additional resources have been developed for species in the Ranunculales, with the aim of elucidating gene function and molecular processes, mainly for studies in evolutionary developmental genetics of flowers and secondary metabolite analysis. The latter may be studied by inducing their production in cell culture systems, providing the cultures with standardized substrates and analyzing their products. These cell culture systems were established for the Ranunculaceae T. thalictroides and Nigella damascena (Smolko and Peretti, 1994; Klimek-Chodacka etal., 2020), and the Papaveraceae E. californica, M. cordata, Corydalis sempervirens, and P. somniferum (Franke and Böhm, 1982; Eilert et al., 1985; Holländer-Czytko et al., 1988; Hauschild et al., 1998). Even more useful are stably transformed cell culture systems, allowing the careful analysis of genes involved in the regulation of biosynthesis. Protocols for these are available for Thalictrum flavum, N. damascena, E. californica, and P. somniferum (Belny et al., 1997; Samanani et al., 2002; Fujii et al., 2007; Mohammed and Masyab, 2020). The analysis of developmental processes can be achieved only in growing plants, ideally using knockout mutants. However, stable transformation of plants and regeneration of the transgenics is a very challenging process, often requiring laborintensive tissue culture steps, and has thus not been established for many Ranunculales species. The notable exceptions here are E. californica, M. cordata, and P. somniferum (Park and Facchini, 2000a, b; Huang etal., 2017; Lotz etal., 2022), but publications of gene function analysis based on regenerated Ranunculales transgenics do not exist to date. An alternative approach to down-regulate gene expression in plants is virus-induced gene silencing (VIGS), which utilizes the plant’s immune system to repress viral transcript synthesis. Specific VIGS vector systems using modified plant viruses were developed to efficiently down-regulate target genes (DineshKumar etal., 2003; Liu etal., 2022). While this is a transient approach requiring careful analysis of the manipulated plants, tissue culture is not necessary, speeding up the process of gene function analysis considerably (Dommes etal., 2019; Rössner et al., 2022). This method is available for Aquilegia coerulea, T. thalictroides, T. clavatum (on dormant tubers), T. dioicum, N. damascena, Delphinium ajacis, E. californica, P. somniferum, and Cysticapnos vesicaria (Hileman etal., 2005; Gould and Kramer, 2007; Wege etal., 2007; Di Stilio etal., 2010; Hidalgo etal., 2012; Wang et al., 2015; Zhao et al., 2023) allowing for the comparative analysis of gene function among species and the assessment of functional conservation (Di Stilio, 2011) Phylogeny of Ranunculales Over the past several decades, tremendous progress has been made in delimiting and elucidating phylogenetic relationships Species Genome available BUSCOaCell/callus culture system Cell culture transformation system Stable transformation Virus-inducedgene silencing Spontaneous mutants Kingdonia uniflora Sun etal. (2020) 90.6 No No No No Lardizabalaceae Akebia trifoliata Huang etal. (2021) 94.0 No No No No Berberidaceae Epimedium pubescens Shen etal. (2022) 89.9 No No No Wang etal. (2017) Epimedium grandiflorumb a Benchmarking Universal Single-Copy Orthologs (BUSCO) percentages are provided as a measure for genome completeness. b Reference genomes are being sequenced and/or expression atlases are being produced by the RanOmics group or are already available via Phytozome (for E. californica). Table 1. Continued Downloaded from https://academic.oup.com/jxb/article/75/7/1800/7477764 by guest on 23 October 2025
Copyedited by: OUPCopyedited by: OUP Ranunculales model lineage | 1805 among the infraordinal taxa within Ranunculales. As currently circumscribed by molecular data, the order consists of seven monophyletic families: Berberidaceae, Circaeasteraceae, Eupteleaceae, Lardizabalaceae, Menispermaceae, Papaveraceae, and Ranunculaceae (Wang etal., 2009; The Angiosperm Phylogeny Group, 2016). Three major clades are recovered: Eupteleaceae, Papaveraceae, and the core Ranunculales (Kim etal., 2004; Wang etal., 2009). The relationships among these three clades are not well resolved, but the majority of phylogenetic analyses recognize the monogeneric Eupteleaceae as the earliest diverging lineage with weak to moderate support (e.g. Kim et al., 2004; Worberg etal., 2007; Wang etal., 2009; Sun etal., 2017; Peng etal., 2023). Within the core Ranunculales, Circaeasteraceae and Lardizabalaceae form a clade, and Menispermaceae, Berberidaceae, and Ranunculaceae form another clade, with Berberidaceae as sister to Ranunculaceae (Kim etal., 2004; Wang etal., 2009; Sun etal., 2017; Peng etal., 2023). The Eupteleaceae include a single genus with two species only, Euptelea pleiosperma and Euptelea polyandra (Cao et al., 2016). Genome sequence or other resources are not available for this genus. Papaveraceae sensu latu contain four subfamilies: Fumarioideae, Hypecoideae, Papaveroideae (including Chelidonieae, Eschscholzieae, and Papavereae), and Pteridophylloideae (Hoot etal., 2015). The position of Pteridophylloideae has been controversial (reviewed by Peng etal., 2023) Recently, a complete genus-level phylogeny was built for Papaveraceae, in which Papaveroideae form a clade, whereas Pteridophylloideae, Hypecoideae, and Fumarioideae form another clade, with Hypecoideae as sister to Fumarioideae; the relationships among 91% of all currently recognized genera in the family are well resolved (Peng etal., 2023). Circaeasteraceae consists of two monotypic genera, Circaeaster and Kingdonia, and it is the sister group to Lardizabalaceae (Wang et al., 2009; Sun et al., 2017). Within Lardizabalaceae (the sister family of Circaeasteraceae), Sargentodoxa, Decaisnea, and Sinofranchetia are successive sister taxa to the other genera (Wang etal., 2009, 2020). Within Menispermaceae, two subfamilies are recognized: Chasmantheroideae and Menispermoideae (Ortiz et al., 2016). Chasmantheroideae comprises Coscinieae and Burasaieae, and Menispermoideae comprises eight tribes, among which Menispermeae is the earliest diverging, followed by Anomospermeae, then Limacieae. Cebatheae, Cissampelideae, Pachygoneae, Spirospermeae, and Tiliacoreae form a clade with strong support, but the relationships among these five tribes are not resolved because they might have diversified rapidly over a period of <6 million years (Wang etal., 2017; Lian etal., 2020). Berberidaceae contain three subfamilies, Podophylloideae, Berberidoideae, and Nandinoideae, corresponding to the chromosome base numbers x=6, 7 and 8, or 10, respectively (Wang etal., 2007, 2009; Sun etal., 2018). Recently, Hsieh etal. (2021) further updated the classification system for this family at the tribal and generic levels. Ranunculaceae (Tamura, 1965, 1993) consists of five subfamilies: Coptidoideae, Glaucidioideae, Hydrastidoideae, Ranunculoideae, and Thalictroideae (Wang et al., 2009). Most studies support Glaucidioideae as sister to the remaining taxa of the family, followed by Hydrastidoideae, then Coptidoideae (e.g. Kim et al., 2004; Wang etal., 2009, 2016; Cossard etal., 2016; Zhai etal., 2019), whereas other studies place Glaucidioideae as sister to Hydrastidoideae (Hoot et al., 1999; Soltis, 2000). Thalictroideae and Ranunculoideae are characterized by the Tand R-type chromosomes, respectively (with R-type being metacentric and T-type telocentric, with only one arm; Wang etal., 2009), but the monophyly of Ranunculoideae remains controversial. Based on eight DNA loci from three genomes, Cossard etal. (2016) placed Thalictroideae in Ranunculoideae, as sister to Adonideae. That was confirmed by a plastid phylogenomic analysis (Zhai etal., 2019), whereas a phylotranscriptomic analysis strongly supports the monophyletic Ranunculoideae (He etal., 2022). He etal. (2022) suggest that the different positions of Adonideae in the nuclear and plastid trees could result from ancient hybridization and/or subsequent introgression events. The currently recognized Ranunculoideae contains 10 tribes, which together with Thalictroideae appear to have diversified rapidly over a period of <14 million years, and perhaps in as little as 1–2 million years (Wang etal., 2016). Fossil record The fossil record of the Ranunculales includes nearly 800 occurrences (Xing etal., 2016), but most of them should be considered with caution. In particular, few reliable fossils have been described from the Cretaceous period (Friis etal., 2011). Three northern hemisphere fossils could illustrate the early diversification of Ranunculales during this period. The flower of Teixeiraea lusitanica from the Cretaceous [~113 million years ago (Ma)] of Portugal is considered to be part of the stem or crown of the Ranunculales without family assignment von Balthazar et al., 2005). Also, from Portugal and with similar age, the flower Kajanthus lusitanicus is the first Cretaceous occurrence of Ranunculales assigned to the family Lardizabalaceae (Mendes etal., 2014). However, a new study considers this flower as more confidently assigned to the crown group of Ranunculales, making it undefined at the family level (Schönenberger etal., 2020). The anatomy of the stem of the liana Atli mornii Smith, Little, Cooper, Burnham, and Stockey from the Late Cretaceous (77– 74 Ma) of Canada allows for the identification of Ranunculales without family affinity, and reinforces the early presence of Ranunculales in Laurasia (Smith et al., 2013). However, the recent description of Santaniella lobata based on fruits and stems from the Cretaceous (Barremian/Aptian, ~125 Ma) of Brazil related to Ranunculales (Gobo etal., 2022) along with the leaf with unknown affinity but close to Ranunculales in shape, named Baderadea pinnatissecta described from the same region (Pessoa etal., 2021), could indicate a Lower Cretaceous Downloaded from https://academic.oup.com/jxb/article/75/7/1800/7477764 by guest on 23 October 2025
Copyedited by: OUPCopyedited by: OUP 1806 | Becker et al. origin of the Ranunculales in Gondwana rather than Laurasia. Nevertheless, additional data from S. lobata indicate that this fossil belongs to angiosperms without certainty about the order (Pessoa etal., 2023). With the exclusion of the monotypic family Circaeasteraceae, the other families are represented in the fossil record (Xing etal., 2016). Although the families of Ranunculales appear to have diverged early on, no Cretaceous fossil can be confidently assigned to any extant family. The unequivocal fossils assigned to a particular family are mostly fruits, seeds, leaves, wood, and pollen from the Paleogene (Friis etal., 2011). The family Berberidaceae is represented by ~100 fossils from the Oligocene to the Pliocene, mainly from North America and Europe, but also from Asia (Friis etal., 2011; Xing etal., 2016; Chen etal., 2020). Fossils of Berberidaceae are represented by only two genera, Mahonia and Berberis, based on leaves and seeds (Xing etal., 2016). Fossils of the Eupteleaceae family are scarce; however, Friis etal. (2011) indicate the presence of a few fossils from this family in the Northern Hemisphere from the Paleocene to the Miocene. The fossil record of Lardizabalaceae was recently reviewed (Wang et al., 2020). During the Cenozoic, fossils attributed to this family come from the Eocene to Miocene of Europe and the USA, as well as from the Miocene of Japan and the Cenozoic of South America. Most of the fossils belong to the genus Sargentodoxa, with the exception of Decaisnea seeds from the Oligocene of Germany and a liana attributed to the family level (Wang etal., 2020). The very diverse woody family Menispermaceae has a very abundant fossil record compared with other Ranunculales families, with many fossil fruits, leaves, and wood having been described (Jacques, 2009; Xing etal., 2016). Several Cretaceous fossils may be credible, such as the morphological genus Menispermites, but need revision (Jacques, 2009). Characteristic endocarps named ‘moonseed’ are traditionally found in North America and Europe (Jacques, 2009), and were also recently found in South America (Herrera etal., 2011; Jud etal., 2018) and Asia (Han et al., 2018, 2020) as early as the Paleocene. Within this family, a total of 44 genera have been found in the fossil record, of which 17 are extant and 27 are extinct (Jacques, 2009). This fossil record attests to a rapid and universal diversification of Menispermaceae during the Paleogene as well as a complex migration of flora during this period. Reliable fossil record of Papaveraceae is meager and is represented, to our knowledge, only by a Corydalis from the Pliocene of Italy (Mai, 1995). The fossil record of the Ranunculaceae family, mostly based on fruits, was revised by Pigg and Devore (2005). Most of these fossils are distributed in Europe and North America, from the Paleocene to the Pliocene, and some seeds were recently found in the Pliocene of China (Huang etal., 2021). It is noteworthy that the fossil record of Ranunculales is relatively sparse in comparison with the present diversity of the order and knowing its ancient evolutionary history. A large part of the extant diversity is represented by plants with herbaceous or climbing habitus, which have low fossilization potential (Friis etal., 2011). Moreover, the potential Ranunculales fossils from the Cretaceous are also difficult to distinguish from indirectly related early-diverging eudicot lineages (e.g. Sun etal., 2011; Pessoa etal., 2021). The Ranunculales fossil record also illustrates a well-known bias in collecting and studies in paleobotany, namely the historical focus on Europe and North America (Xing et al., 2016). Recent discoveries, particularly from South America and Asia, may strengthen the fossil record of the order in the future. Distribution and ecological niches The order Ranunculales comprises ~4500 species, primarily occupying temperate areas of the world, with few members cosmopolitan or reaching into the tropics. Namely, the two species of Euptelea (Eupteleaceae) occur in Japan between 400 m and 1500 m (E. polyandra) and from India to China between 900 m and 3600 m (E.3 pleiosperma; Endress, 1993). In contrast, the Papaveraceae with ~430 species in 42 genera are primarily distributed in the northern hemisphere with few exceptions, including Papaver aculeatum in South Africa, and the genus Bocconia that reaches central and South America (Kadereit, 1993). The Fumarioideae are concentrated in the Sino-Himalayan and Mediterranean regions, with occurrences in South Africa and North America (Lidén, 1993a). Both Papavereae and Chelidonieae (Papaveroideae) contain Old and New World genera. Most Papavereae in the New World inhabit western North America, while the Old World genera are concentrated in southwest and central Asia, and the Mediterranean. The genus Papaver is broadly distributed in the Old and the New World. The Eschscholzieae (Papaveroideae) are found in the New World and almost exclusively in Pacific North America. Hunnemania is present in the east of Mexico. Most Papavereae and Eschscholzieae are found in open vegetation arid and warm climates, with a few exceptions that have colonized arctic areas. Conversely, the Chelidonieae of the New World occupy regions in Northeast America with the exceptions of Bocconia (Central and South America) and Glaucium and Dicranostigma (West and Central Asia). They can inhabit dry open areas (Glaucium, Dicranostigma, and Macleaya) or deciduous forests (Hylomecon, Sanguinaria, and Stylophorum). The only species of Pteridophyllum, Pteridophyllum racemosum, is a Japanese endemic (Lidén, 1993b). Species of Papaveraceae selected as part of the RanOmics project include: Corydalis tomentella, Capnoides sempervirens, Eschscholzia californica, Macleaya cordata, Papaver rhoeas, Papaver setigerum, Papaver somniferum, and Pteridophyllum racemosum. Corydalis tomentella is a perennial, native to China, that grows in rock crevices, between 700 m and 1000 m. The plant itself reaches 15–20 cm, it has characteristic golden yellow flowers in dense inflorescences, and it can tolerate freezing temperatures (http://www.efloras.org/flora_page.aspx?flora_id=2). Capnoides sempervirens (pale corydalis or rock harlequin) is a Downloaded from https://academic.oup.com/jxb/article/75/7/1800/7477764 by guest on 23 October 2025
Copyedited by: OUPCopyedited by: OUP Ranunculales model lineage | 1807 biennial plant from the mid-latitudes of North America where it grows on exposed ridges and rocky outcrops (Sprengelmeyer and Rebertus, 2015), and it produces monosymmetric flowers, which are exceptional in that they are in a terminal position (Hidalgo and Gleissberg, 2010). Eschscholzia californica is a small herb able to grow as annual or perennial with native ranges from Northern California to Southwestern Mexico, with cymose inflorescences and flowers with deciduous sepals and characteristic yellow petals (Becker etal., 2023). Macleaya cordata is a herbaceous, perennial native to China, Japan, and Taiwan, unusual in that it can reach sizes of up to 3 m, it spreads by rhizomes, and it has massive inflorescences of showy but apetalous flowers (Kadereit, 1993; Arango-Ocampo etal., 2016). Macleaya cordata is the source of alkaloids with broad uses as detoxifiers, antimicrobials, and insecticidals (Liu etal., 2017). All Papaver species are herbs with cymes carrying large showy flowers. Papaver somniferum is the source of opium, and its center of domestication was the Mediterranean basin (Salavert etal., 2020; Hong etal., 2022). Numerous biochemical accounts with emphasis on the production of BIAs are available for different landraces (Pei etal., 2021), and two features have been linked to domestication, namely changes in capsule dehiscence and seed size (Zohary etal., 2012). Interestingly, morphine, codeine, and thebaine are lacking in capsules of the closely related and geographically overlapping P. setigerum (La Valva etal., 1985). Albeit the two species were thought to be part of the same taxonomic unit, P. somniferum is 30–150 cm high, self-pollinated, and diploid, while P. setigerum is 60 cm high, a field weed occurring in disturbed grounds that can be diploid or tetraploid (Hammer 1977; Jesus etal., 2021). Papaver rhoeas, the red poppy, is a remarkable species with exceptional beauty that has reproduced and expanded its native range across the Mediterranean as an agricultural weed (Colledge et al., 2004). Papaver rhoeas is a self-incompatible herb, currently pollinated by bees, flies, and beetles (McNaughton and Harper, 1960; Foote, 1994). Finally, the rare P. racemosum is a herb with leaves of astonishing shape convergent to those of ferns, is only found in Japan, and it grows between 1000 m and 2000 m in coniferous forests. It shares with the rest of Papaveraceae the caducous sepals and the dimerous floral organization, despite the unusual leaf phenotypes (Lidén, 1993a, b). The Lardizabalaceae (35 species in eight genera) are primarily present in Japan, the Sino Himalayan mountains, Central and East China, and Vietnam. All genera are woody vines in subtropical evergreen forests or warm temperate green forests. Only Lardizabala and Boquila are endemic to temperate forests of Central and South Chile (Cheng-Yih and Kubitzki, 1993). Their most prominent member is Akebia trifoliata, a deciduous to evergreen twining vine, reaching up to 10 m in height with functionally unisexual flowers. Its berries are a rich source of vitamin C and pectin, and the seeds contain a high percentage of unsaturated fatty acids; the species is widely advertised as a new fruit crop. Akebia trifoliata consists of three subspecies, all with different but overlapping distributions ranging from subtropical to temperate regions from 20 m up to 2800 m in elevation in China and Taiwan (Zhang etal., 2021; Zou etal., 2022). Only A. trifoliata is a member of the RanOmics project. Conversely, the Circaeasteraceae (two species) are herbs. Two genera are recognized: Circaeaster is present in India, Nepal, and China, and grows in moist coniferous forests between 1200 m and 5000 m. Kingdonia uniflora, on the other hand, is endemic to China (provinces of Shaanxi, Sichuan, Gansu, and Yunnan) between 2800 m and 3200 m (Cheng-Yih and Kubitzki, 1993) and is selected as the representative species of Circaeasteraceae for the RanOmics project. The Menispermaceae consist of ~450 species in 71 genera, including many woody climbers, and rarely trees, shrubs, or herbs. They are of cosmopolitan distribution, mostly confined to the tropical lowlands in the Old and the New World. They are extremely diverse in their habitats and found in Africa and Southeast Asia (Stephania), extra tropical North America (Cocculus and Menispermum), the Mediterranean (Cocculus), Japan (Cocculus and Stephania), and South America (Abuta and Chondrodendron) (Kessler, 1993; Ortiz etal., 2007). Species of Berberidaceae selected as part of the RanOmics project include Epimedium grandiflorum and Epimedium pubescens. The Berberidaceae include ~650 species organized in 14–17 genera. They are herbs or woody shrubs, often a component of mesophytic forests in East Asia, Northeast America (Achlys, Diphylleia, Jeffersonia, Podophyllum, and Sinopodophyllum), Andean South America (Berberis); even desert xerophytes are found in Southwest Asia. Members of Berberis are also found in South America, from Colombia to Chile, Juan Fernandez Islands, and Argentina (Loconte, 1993). In addition, a few species of Berberis have become invasive in North America and South Africa (Keet etal., 2016). The pharmaceutically and horticulturally relevant Epimedium genus includes only herbaceous species growing mainly in woodlands. Its center of diversity is East Asia, with most species native to China. However, some species grow in the Alps, the Balkan region, Algeria, Caucasia, Japan, east Russia, and Kashmir (Zhang etal., 2022). Epimedium pubescens is native to the Chinese provinces Anhui, Jiangxi, and Sichuan (Stearn etal., 2002). Epimedium grandiflorum, a species with large flowers comprising curved nectar spurs, grows in Japan, North Korea, and South China, and varies greatly in flower color between white, light yellow, and purple-pink (Stearn etal., 2002). The Ranunculaceae is a cosmopolitan family with ~2500 speciess in 59 genera. With large preferences for temperate or cool climates, they are a rare element in the tropics (Chartier etal., 2016). The most broadly distributed elements in northern and southern hemispheres include Anemone, Caltha, Clematis, Myosurus, Ranunculus, and Thalictrum. A total of 44 genera are present in East Asia, 24 in Europe, with few genera in temperate North America and in Highlands in South America (Tamura, 1993). Species of Ranunculaceae selected as part of the RanOmics project include Coptis chinensis, Aquilegia coerulea, Aquilegia oxysepala, Thalictrum thalictroides, Nigella damascena, Staphisagria picta, and Hydrastis canadensis. Downloaded from https://academic.oup.com/jxb/article/75/7/1800/7477764 by guest on 23 October 2025
Copyedited by: OUPCopyedited by: OUP 1808 | Becker et al. In many phylogenies, H. canadensis or goldenseal is the sister species to all remaining Ranunculaceae. It is native to the eastern deciduous forests of North America. It grows in dense patches resulting from clonal growth via rhizome and lateral root formations (Sanders and McGraw, 2005). The rhizomes of this species are highly prized as a food supplement and as a traditional remedy for diverse conditions, including wound healing, digestive disorders, and cancer, with berberine as the pharmacologically most active ingredient (Mandal etal., 2020). Several H. canadensis populations are under serious threat caused by commercial and private harvesting of natural populations (Albrecht and McCarthy, 2006). Sister to the Thalictroideae and Ranunculoideae are the Coptidoideae, with Coptis chinensis as a RanOmics species representative. The species has an at least 2000 year long history as traditional Chinese medicine, with berberine also as the dominant alkaloid. The rhizomes of C. chinensis are harvested, and it is cultivated in several Chinese provinces in shady, moist, and cool mountainous regions between 1200 m and 1800 m (Chen etal., 2021). Coptis chinensis is endangered in the wild and its remaining populations are found in the woodlands of central China at altitudes of 500–2000 m. This species, like H. canadensis, suffers from harvesting of the rhizomes (He etal., 2007). Nigella damascena (commonly known as love-in-the-mist) is an annual herbaceous weedy species growing throughout the Mediterranean. As a popular ornamental plant, it was most probably distributed by seeds along ancient trade routes (Heiss and Oeggl, 2005). Interestingly, a mutant that lost petal identity and has numerous petaloid tepals was described as early as in 1601 (Clusius, 1601). Staphisagria picta is a species endemic to Corsica, Sardinia, and Majorca, growing between 150 m and 600 m in open grasslands (Orellana etal., 2009). Aquilegia oxysepala is broadly found throughout Southeastern China and grows in open patches, along roadsides and forest margins at low altitudes (Li etal., 2014). Aquilegia coerulea (also described as Aquilegia caerulea) also has a large area of distribution, stretching across the Southern and central Rocky Mountains of western North America from 2100 m to 3700 m altitude (Miller, 1981). For genetic studies, mainly the commercially available, fast cycling cultivar ‘Origami’ is used (Sharma and Kramer, 2013). Thalictrum thalictroides (Ranunculaceae, also known as Anemonella thalictroides, commonly called rue anemone) is a spring ephemeral growing on streams and open woods in the Eastern USA (Lubbers and Christensen, 1986). Taken together, the Ranunculales species for which genomic resources of various kinds are available occupy diverse habitats that range from dry Mediterranean islands (S. picta) over high altitudes (A. coerulea), to damp temperate forests (P. racemosum). Some species are abundant (N. damascena) or even invasive (E. californica), but several Ranunculales are rare and threatened in the wild (H. canadensis, C. chinensis, S. picta, and P. racemosum). Floral diversity in Ranunculales Floral structure and perianth in families of Ranunculales Like floral phyllotaxis and symmetry, perianth organ identity, development, and function(s) are extremely diverse in Ranunculales, and range from absent to undifferentiated tepals, or more or less differentiated and petaloid sepals and modified and nectariferous petals (Fig. 2). For instance, flowers of Fig. 2. Simplified phylogeny of Ranunculales showing ancestral floral traits of the Ranunculales families. Downloaded from https://academic.oup.com/jxb/article/75/7/1800/7477764 by guest on 23 October 2025
Copyedited by: OUPCopyedited by: OUP Ranunculales model lineage | 1815 (Fig. 4). Achenes, dry indehiscent fruits, were independently acquired in Circaeasteraceae and some Ranunculaceae. Regarding the genetic bases for fruit development, there are a number of genes whose function seems to be maintained in both Papaveraceae and Arabidopsis. They include FRUITFULL (FUL) genes largely expressed in the fruit wall in E. californica and P. somniferum. When FUL genes are down-regulated, fruit defects include premature rupture of the fruit wall and numerous cell proliferation defects, especially in the endocarp (Pabón-Mora etal., 2012). APETALA2 (AP2) genes are, on the other hand, very different. The two copies show overlapping expression only in the commissural tissue, and one of the homologs is also expressed in the fruit wall. Very important is the fact that both copies are absent from the dehiscence zone (DZ). These expression patterns suggest a role for AP2 genes in fruit wall development, most probably acting as repressors of DZ-specific genes (Zumajo-Cardona etal., 2021). Further, the E. californica homolog of CRC (EcCRC) is required for adaxial gynoecium tissue development, and down-regulation leads to a complete abolishment of the DZ (Orashakova etal., 2009). Genes probably controlling the formation of the DZ in Papaveraceae are SPATULA/ALCATRAZ homologs specifically Fig. 4. Ancestral state reconstruction of gynoecium (left) and fruit (right) characters based on a phylogeny using rbcL as the marker gene. Trait descriptions are from Cheng-Yih and Kubitzki (1993), Endress (1993), Kadereit (1993), Lidén (1993a, b), Loconte (1993), and Tamura (1993). Downloaded from https://academic.oup.com/jxb/article/75/7/1800/7477764 by guest on 23 October 2025
Copyedited by: OUP 1816 | Becker et al. restricted to those layers (Zumajo-Cardona etal., 2017), acting together with REPLUMLESS genes, which were observed in the DZ not only in Bocconia, but also in Papaver, suggesting that this is a common putative role for many Papaveraceae (ZumajoCardona et al., 2018). In A. thaliana, INDEHISCENT and SHATTERPROOF1 and 2 are essential for the formation of the DZ. However, as their orthologs do not exist in Ranunculales (Zahn etal., 2006; Pabón-Mora etal., 2014), the dry dehiscent fruits predominant in the Ranunculales require a gene regulatory network very different from that of A. thaliana. Conclusions This review has highlighted the Ranunculales as an emerging model lineage for comparative analysis of morphological and metabolic traits in angiosperms, pointing out recent developments in the field of genomics and genetic manipulation of several members from diverse families. The amazing morphological diversity of Ranunculales raises the question of the underlying genetic bases (particularly concerning convergent traits), still largely unexplored, but also the question of floral integration (whether traits evolve independently from each other or in a correlated manner). Addressing these questions in Ranunculales, an order with a key phylogenetic position, may contribute to a better understanding of the drivers of morphological evolution in angiosperms as a whole. Combining a solid phylogeny and fossils for its calibration, molecular tools and genetic resources, together with high morphological diversity, convergent evolution of characters, frequent switching between reproductive systems, and developmental trajectories and functions of perianth organs, the Ranunculales order offers new avenues for investigations into plant evolution and adaptation. Acknowledgements The authors thank Annalena Kurzweil (Giessen, Germany) for support during the writing process. Author contributions AB: conceptualization; CD, FJ, VdS, and AB: review and editing. All authors participated in writing the original draft, Conflict of interest The authors declare no conflict of interest. Funding Work in AB’s group on E. californica and on genomic resources of Ranunculales was continuously funded by the DFG (German Research Foundation, grants BE2547/3-1; 6-1; 6-2; 7-2; 14-1; 24-1, the RanOmics project is funded by 27-1). VD was funded by the National Science Foundation (USA), Division of Environmental Biology (Opportunities for Promoting Understanding through Synthesis—Mid-Career Synthesis) grant no. 1911539. YG is supported by National Science Foundation (USA) Postdoctoral Research Fellowships in Biology Program under grant no. 2305493. YG and EMK are supported by National Science Foundation (USA) EDGE Award IOS no. 2128195. 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