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Research Article
A new phylogeny of Rumex (Polygonaceae) adds evolutionary context to the diversity of reproductive systems present in the genus
expand article infoKirstie D. Grant, Daniel Koenemann§, Janet Mansaray|, Aisha Ahmed§, Hamid Khamar#, Jalal El Oualidi#, Janelle M. Burke§
‡ Florida Agricultural & Mechanical University, Tallahassee, United States of America
§ Howard University, Washington, United States of America
| Louisiana State University, Baton Rouge, United States of America
¶ Université Ibn Tofail, Kénitra, Morocco
# Université Mohammed V de Rabat, Rabat, Morocco
Open Access

Abstract

Rumex is one of about 50 genera in the knotweed family, Polygonaceae. The genus comprises about 200 species with bisexual, or more commonly, unisexual flowers, with the species displaying monoecious, dioecious, synoecious (hermaphroditic) or polygamous reproductive systems. Some of the dioecious species have heteromorphic sex chromosomes, which is rare amongst angiosperms. We here present a plastid phylogeny of 67 species, representing all four subgenera. For this study, we used three chloroplast markers, rbcL, trnH-psbA, trnL-F and dense taxon sampling to reconstruct the most comprehensive molecular phylogeny of Rumex to date. The reconstructed phylogeny for this work resolves six major clades and one large grade in Rumex subg. Rumex. In addition, the species with known dioecious reproductive systems are resolved within a broader clade we term “the dioecious clade”. These results suggest that the species with divergent reproductive systems are more closely related to each other than to other species comprising the rest of the Rumex genus.

Keywords

Dioecious, Emex, heteromorphic sex chromosome systems, monoecious, synoecious

Introduction

Commonly known as docks and sorrels, Rumex L. (Polygonaceae) is a relatively large genus. Rumex encompasses four circumscribed subgenera, approximately 200 species and hundreds of described subspecies or varieties. Many species in Rumex are cosmopolitan in nature, spanning six continents of the world. However, many individual species are either regionally endemic, native or introduced on particular continents (Rechinger 1937).

The cosmopolitan distribution of Rumex species is indicative of their ability to thrive in a wide variety of environmental conditions. Described species are just as recurrent in dry and sandy soils as they are in marshes and cultivated fields, spanning the arctic, subarctic, boreal, temperate, tropical and subtropical localities (Löve and Kapoor 1967). Although several biological species demonstrate little to no niche preference (e.g. Rumex crispus L., Rumex obtusifolius L.), there are others that exhibit exceedingly precise ecological requirements (e.g. Rumex bipinnatus L.f., Rumex pictus Forrsk.). The large variation in the distribution of Rumex species might also account for the large deviation observed in the morphology of these species (Fig. 1), whereby some reach almost seven metres in height and others rarely exceed a few centimetres (Rechinger 1949; Löve and Kapoor 1967; Rechinger 1990).

Figure 1. 

Depiction of morphological variation amongst the different subgenera of Rumex. A Rumex acetosella growing in Virginia, USA (subg. Acetosella) B Rumex thyrsoides growing in Morocco (subg. Acetosa) C Rumex nervosus growing in Ethiopia (subg. Acetosa) D Rumex obtusifolius growing in New York, USA (subg. Rumex) E Rumex bucephalophorus collected on the Moroccan coast (subg. Platypodium) F Rumex papilio growing in Morocco (subg. Acetosa). All photo credits J.M. Burke.

In the 20th Century, progress in the taxonomic and cytological study of Rumex was largely accomplished by two researchers: Áskell Löve and Karl Heinz Rechinger (Rechinger 1937; Rechinger 1954a; Löve and Kapoor 1967). Löve extensively documented the cytological diversity of Rumex and he proposed a generic status for Acetosa and Acetosella (the groups with species bearing heteromorphic sex chromosomes) and subgeneric status for Axillares and Platypodium. Löve also considered Rumex to be composed of several smaller genera corresponding to a number of cytotypes (Löve 1957; Löve and Kapoor 1967; Mariotti et al. 2006, 2009).

Over the course of his career, Rechinger effectively monographed Rumex, using plant morphology and geographic distribution in his taxonomic treatments (Rechinger 1933, 1937, 1939, 1949, 1954a, b, 1984, 1990; Brandbyge and Rechinger 1989). By the mid-1900s, Rechinger had proposed a subgeneric status for Platypodium and maintained Acetosa, Acetosella and Lapathum as comparable subgenera (Rechinger 1954a; Table 1). Rechinger chose to retain Rumex as a single genus.

Table 1.

Summary of the recognised subgenera in Rumex, with species diversity and reproductive systems present.

Subgenus No. of species Sexual system Sex chromosomes
Acetosa 41 Dioecious, Gynodioecious, Polygamous Yes (in part)- XX/XY1Y2
Acetosella 5 Dioecious (rarely polygamous) Yes- XX/XY
Rumex (= Lapathum) 126 Synoecious, Monoecious No
Platypodium 1 Synoecious No

The reproductive systems of Rumex species vary extensively. Species of Rumex exhibit synoecious (hermaphroditic), monoecious, dioecious and polygamous reproductive systems (Rechinger 1949; Rechinger 1954a; Löve and Kapoor 1967; Mosyakin 2005; Navajas-Pérez et al. 2005). Most of the reproductive system diversity has been described in subgenera Acetosa or Acetosella. In particular, most species in these subgenera are dioecious (Rechinger 1937, 1949, 1954a, 1984). A few species in subgenus Rumex have variable systems, especially between synoecy and monoecy (e.g. Rumex crispus, J. Burke, pers. obs.). There are also three species of Rumex endemic to the Hawaiian Islands (Rumex albescens Hillebr., R. giganteus Aiton and R. skottsbergii O. Deg. & I. Deg.), which are all monoecious (Wagner et al. 1999).

Rumex has two different sex chromosome systems exhibited in many of the dioecious species, classified in Rumex subg. Acetosa and Rumex subg. Acetosella. In Rumex, the documented sex chromosomes are heteromorphic. Two sex-determining chromosomal mechanisms are known: XX/XY and XX/XY1Y2 (Löve 1940, 1942,1943, 1944; Löve and Löve 1948; Shibata et al. 1999, 2000; Navajas-Pérez et al. 2005; Cunado et al. 2007; Ming et al. 2011). The XX/XY1Y2 system is dosage-dependent and plant sex is based on the autosome to sex-chromosome ratio. In this system, female individuals have 14 chromosomes and male individuals have 15 chromosomes (Löve 1940, 1944; Löve and Kapoor1967; Navajas-Pérez et al. 2005).

Recent molecular phylogenetic work has sought to resolve the placement of Rumex in the Polygonaceae more broadly (Sanchez and Kron 2008; Sanchez et al. 2009; Burke et al. 2010; Burke and Sanchez 2011; Sanchez et al. 2011; Schuster et al. 2011, 2013, 2015). These studies have placed Rumex alongside the other Rumices of Campderá (Emex and Oxyria), with the addition of Rheum as either sister to Oxyria (Burke et al. 2010; Schuster et al. 2011) or to Rumex + Emex (Schuster et al. 2013, 2015). One area that lacks clarity has been the placement of Emex, which sometimes appears to be nested within Rumex (e.g. Sanchez et al. 2011) and is sometimes placed as sister to Rumex (e.g. Burke et al. 2010). Moreover, the relationships of species within Rumex, including the relationship between Rumex and Emex, continue to be poorly understood due to insufficient sampling and paucity of data. To date, the relationships amongst species placed within Rechinger’s subgenus Rumex are particularly obscure.

Here we present a new phylogeny of Rumex, constructed using three plastid gene regions (trnH-psbA, rbcL and trnL-F) and 67 Rumex species. We have used this phylogeny to test the placement and monophyly of its circumscribed subgenera, as well as discuss the broad patterns in the evolution of reproductive systems within Rumex.

Materials and methods

Taxon sampling and DNA Isolation

DNA was isolated from 109 accessions, representing 67 Rumex species. Of the 109 included accessions, a total of 99 Rumex accessions, six Rheum L. species, three Emex L. accessions and one species of Persicaria L. (Mill.) are represented. Persicaria virginiana (L.) Gaertn., Rheum alexandrae Batalin, Rheum emodii Wall., Rheum nobile Hook. f. & Thomson, Rheum officinale Baill., Rheum palmatum L. and Rheum rhabarbarum L. were included as outgroup species. Additional plant samples were obtained through the GenBank sequence database (Appendix A1). Samples were taken from a combination of herbarium specimens (K, NY, OSC, RAB, US), field collections and cultivated samples from collaborators. Herbarium acronyms follow the Index Herbariorum (Thiers 2019).

All fresh leaf samples were dried using silica gel. Plant tissue was homogenised using the FastPrep-24 5G Sample Preparation System (M. P. Biomedicals, LLC Santa Ana CA, USA). Total genomic DNA was extracted from herbarium specimen-sampled and silica-dried leaf tissues using a BIOLINE ISOLATE II Plant DNA Kit (Cat No. BIO-52070). Modification for herbarium material proceeded as follows: Cell lysis was carried out using 300 µl of buffer (PA1 or PA2) and 30 µl of proteinase K (20 µg/ml) and incubated for 18 hours at 65 °C on an orbital shaker.

Marker selection

For this first comprehensive phylogeny of the genus, we focused on plastid marker selection. Previous authors utilised nrITS as a nuclear marker (Schuster et al. 2011; Schuster et al. 2015). However, we did not utilise nrITS for this phylogeny due to a number of issues that would interfere with accurate reconstruction of evolutionary relationships: 1) nrITS is extremely variable and difficult to align (66% of nrITS sequence data was excluded in Schuster et al. [2015] publication) and 2) Due to widespread polyploidy documented in multiple Rumex species, sequences of nrITS would not necessarily be low copy and there would be substantial issues with paralogy and orthology across multiple polyploidy events.

For plastid marker selection, we screened multiple markers that had previously been used in Polygonaceae reconstruction (Burke et al. 2010; Burke and Sanchez 2011; Koenemann and Burke 2020). We selected markers that both showed sufficient variation across the genus and were easily amplified for most taxa.

PCR amplification and sequencing

Amplification of DNA markers was completed for three plastid regions: rbcL, trnH-psbA and trnL-F (Table 2). rbcL was amplified using the following PCR conditions: 94 °C for 1 min, followed by 34 cycles of 94 °C/15 s, 54 °C/15 s and 72 °C/30 s and a final extension period of 5 min at 72 °C. trnH-psbA was amplified using the following PCR conditions: 94 °C for 2 min, followed by 34 cycles of 94 °C/30 s, 55 °C/30 s and 72 °C/30 s and a final extension period of 7 min at 72 °C. trnL-F was amplified using the following PCR conditions: 80 °C for 5 min, followed by 34 cycles of 94 °C/1 min, 55 °C/1 min and 72 °C/2 min and a final extension period of 5 min at 72 °C. PCR and gel electrophoresis were performed following standard protocols with no special conditions. PCR experiments were performed separately with only fresh or only herbarium material to help prevent cross-contamination.

Table 2.

Gene regions used: name of primers, total length of region, % parsimony informative characters.

Gene region Reference Primer names Total aligned length PIC (%)
rbcL Fazekas et al 2008 rbcLF, rbcLR 539 24 (4.5)
trnH-psbA Shaw 2007 psbA, trnH 596 132 (22.1)
3trnL-F Shaw 2005 3’trnLUAAF, trnF GAA 442 65 (14.7)
Combined 1577 221 (14.0)

PCR amplicons were sent to Eurofins Genomics (Louisville, KY) for Sanger sequencing. Sequences were edited using Geneious v. 10 (Biomatters Ltd.). Reviewed sequences were aligned with MUSCLE (Edgar 2004) and concatenated using MESQUITE (Maddison 2005).

Phylogeny reconstruction

All phylogenetic analyses were completed using the CIPRES Science Gateway v. 3.3 (Miller et al. 2010). Prior to the phylogenetic reconstructions, we performed ModelTest-NG (Darriba et al. 2020) for the concatenated matrix to determine the suggested model of evolution. ModelTest-NG indicated that the best fit was the General Time Reversible (GTR) model.

We performed Maximum Likelihood (ML) phylogeny reconstruction using GARLI v. 2.01.1067 (Zwickl 2006). We used the default GARLI parameters with the following exceptions: we performed 1000 search replications (10 iterations of 100 search replicates). In order to better search tree space, we increased the attachments per taxon setting to 150 and extended the generations without improvement parameter to 50000. To evaluate support for phylogenetic relationships, statistical bootstrapping was performed, specifying only one search replicate per bootstrap iteration for 100 iterations. All bootstrap trees were downloaded and used to generate a majority rule consensus tree in MESQUITE (Maddison 2005). The consensus tree was visualised in FigTree version 1.4.3 (Rambaut 2014).

We performed Bayesian Inference phylogeny reconstruction in MrBayes 3.2.7a (Ronquist et al. 2012). The priors were set to the defaults (Dirichlet). We set the seed number at 123. We conducted two independent Markov Chain Monte Carlo (MCMC) runs, each with four chains employing BEAGLE library acceleration (as recommended by CIPRES). Each MCMC run was set to complete 5 million generations, with trees sampled every 1,000 generations. The first 25% of trees in each run were discarded as burn-in. MrBayes then synthesised the two independent runs and extracted the majority rule consensus tree with posterior probabilities.

Posterior probability and bootstrap values were visualised using FigTree version 1.4.3 (Rambaut 2014) and MESQUITE (Maddison 2005). Posterior probabilities above 90% and bootstrap support values above 70% were considered significant and annotated in the final phylogeny.

Results

The most likely tree was generated using 109 specimen accessions. This included seven outgroup species, three accessions of Emex and 99 accessions of Rumex. The present phylogeny represents 67 Rumex species, more than twice the number of species of Rumex sampled in previous phylogenies (31 species in Navajas-Pérez et al. 2005; 13 species in Schuster et al. 2015). A total of 47 sequences were missing from the final matrix, yielding 14.4% missing data in the final analysis (Grant 2022). Table 2 summarises the variability of each of the gene regions. The most variable region was trnH-psbA, which consisted of 22.1% parsimony informative characters. The least variable region was rbcL which consisted of 4.5% parsimony informative characters.

The most likely tree recovered by GARLI received a likelihood score of Ln = -5767.548440.

The genus Rumex was recovered as monophyletic with strong support (100 Bayesian Posterior Probability/98 Maximum Likelihood Bootstrap) (Fig. 2). The analysis did not recover Rumex subgenus Rumex, the subgenus with the most species diversity, as monophyletic. In our phylogeny, species of subgenus Rumex form a grade at the base of the tree (“Basal Grade” – Fig. 2). Emex was recovered as monophyletic, just above the Basal Grade and sister to the dioecious clade. While the results indicate strong support for the relationship between the known Emex species, E. australis and E. spinosa (100/98), they are conflicting and show poor support for the placement of Emex within Rumex. Posterior probability support for the placement of Emex is only 52% and the most likely GARLI tree placed Emex within the Basal Grade of subgenus Rumex. Furthermore, different gene regions reconstructed conflicting topologies for the placement of Emex. The rbcL phlyogeny placed Emex within Rumex subgenus Rumex (50% bootstrap support). Both trnh-psbA and trnL-F placed Emex as sister to the Rumex genus (trnh-psbA < 50% bootstrap support and trnL-F 91% bootstrap support) (results not shown).

Figure 2. 

Bayesian phylogenetic reconstruction for Rumex species using three chloroplast sequences (rbcL, trnH-psbA and trnL-F). Thickened branch indicates simultaneous posterior probability above 90% and bootstrap support above 70%. Exact support values are indicated at important nodes (Bayesian Posterior Probability/Maximum Likelihood Bootstrap). Outgroup species (Rheum and Persicaria) are shown in blue. Rumex species, traditionally placed in subgenus Rumex, are shown in red. Species, traditionally placed in the sister genus Emex, are shown in black. Rumex species, traditionally placed in subgenus Acetosa, are shown in gold. Rumex species, traditionally placed in subgenus Platypodium, are shown in purple. Rumex species, traditionally placed in subgenus Acetosella, are shown in green. The asterisk denotes the transition to dioecy “Dioecious Clade” referenced in the text.

The remaining taxa, comprising the subgenera Acetosa, Acetosella and Platypodium form a highly supported (99/80) monophyletic group (Fig. 2). This group is denoted as “the dioecious clade” because it is here that we see the initial transition to dioecy of the known dioecious Rumex species resolved in this group. The relationships of the clades within this group are also well-supported. Our recovered phylogenetic tree did not recover subgenus Acetosa as monophyletic. Within the dioecious clade, subgenus Acetosa is comprised of three well-supported, monophyletic groups, Clade 2 (100/97), Clade 3 (100/78) and Clade 4 (100/97) and is nested below a pair of clades, represented by subgenus Platypodium (Clade 5) and subgenus Acetosella (Clade 6). The pair (Platypodium + Acetosella) is also well supported (100/81). Subgenus Platypoidium was recovered as monophyletic with strong support (100/100) and consists of four accessions of its only circumscribed species: Rumex bucephalophorus. Species in subgenus Acetosella were recovered together with strong support (100/89), but the inclusion of Rumex hastatulus means the subgenus was not recovered as monophyletic.

In addition to corresponding largely to the established subgeneric system, the topology also largely corresponds to the diversity of the reproductive and sex chromosome systems present in Rumex. Species in subgenus Rumex (Basal Grade) are mostly hermaphroditic with no documented heteromorphic sex chromosomes. With no documented heteromorphic sex chromosomes, Emex is also represented as a clade and consists of purely monoecious species. Subgenus Acetosa consists entirely of dioecious species, with some members exhibiting the sex chromosome system XX/XY1Y2. Subgenus Platypodium, another hermaphroditic group with no reported sex chromosomes, is nested between subgenera Acetosa and Acetosella. Subgenus Acetosella consists of species that are both dioecious and have the sex chromosome system XX/XY.

Discussion

Our results produced a phylogeny of Rumex, with six major clades and one grade, largely congruent with Rechinger’s subgeneric classification. The placement of Emex conflicted, based on the molecular markers used. In our phylogeny, it is sister to the dioecious clade, but without strong support.

Within the phylogeny, the basal grade is mostly made up of species from Rumex subgenus Rumex. That subgenus Rumex was recovered as a grade rather than a clade is not surprising given the known extensive hybridisation amongst species of this subgenus. This phenomenon most certainly contributed to the lack of resolution in species-level relationships within subgenus Rumex. Additionally, although hybridisation between species in subgenus Rumex and species in the other subgenera are not well documented, it is possible that such hybrids exist and serve to hinder our ability to distinguish subgenus Rumex as a clade. We suspect that increased taxon sampling and genetic data, especially from the nuclear genome, will help to resolve relationships amongst species in subgenus Rumex.

Although dioecious, the species included in Clade 2 and Clade 3 have no reported heteromorphic sex chromosome systems. The species included in Clade 4 exhibit a complex sex chromosome system (XX/XY1Y2). This placement suggests that this heteromorphic sex chromosome system was derived from dioecious ancestors. The genetic origin of heteromorphic sex chromosomes in Rumex is beyond the scope of this manuscript, but this result provides a framework to investigate potentially intermediary taxa that may contain homomorphic or transitionary sex chromosome systems.

Subgenus Platypodium (Clade 5) was resolved as monophyletic and nested within “the dioecious clade”. Based on its plant and chromosome morphology, earlier studies concerning Rumex bucephalophorus have referred to it as the link between subgenus Rumex, which is predominantly synoecious and subgenus Acetosella, which is predominantly dioecious (Löve 1944). Although morphologically variable, R. bucephalophorus consistently exhibits a synoecious reproductive system. Its derivation from amongst the dioecious species in this phylogeny suggests a reversal from a dioecious condition.

Subgenus Acetosella (Clade 6) was not recovered as monophyletic. Known dioecious species, R. hastatulus, of subgenus Acetosa is nested within subgenus Acetosella. Rumex hastatulus is documented to exhibit two distinct karyotypes: a complex sex chromosome system (XX/XY1Y2, North Carolina karyotype) which is characteristic of subgenus Acetosa and the simple sex chromosome system (XX/XY, Texas karyotype) which is characteristic of subgenus Acetosella (Navajas-Pérez et al. 2005; Mariotti et al. 2009; Hough et al. 2014). In addition, Rechinger’s 1937 treatment indicates a polygamous reproductive system for R. hastatulus (Rechinger 1937). Given the variability found within this species, R. hastatulus could have been placed in either subgenus (Acetosa or Acetosella), where species appear to have diversified according to the type of sex chromosome system they exhibit. This finding suggests the plasticity of reproductive and sex chromosome systems within Rumex, as a single species can exhibit two different karyotypes.

One of the striking features of the phylogeny recovered in this study is its congruence with the taxonomic system established by Rechinger (Rechinger 1933, 1937, 1939, 1949, 1954a, 1954b, 1984, 1990). Rechinger retained the diversity of species as a single genus, but divided them into four subgenera: Rumex (Lapathum), Platypodium, Acetosa and Acetosella. Each subgenus is prominently present in the topology. Subgenus Platypodium is monophyletic. Subgenus Acetosella is monophyletic even with the inclusion of Rumex hastatulus, whose placement has been ambiguous. The two largest subgenera, Acetosa and Rumex, were recovered as grades. The grade of subgenus Acetosa is well-resolved and well-supported. The grade of subgenus Rumex is both less well-resolved and less well-supported. The recovered topology, nevertheless, serves to confirm the major relationships amongst species in the genus, relationships for which Rechinger had proposed using only morphology.

In all, this work has provided a reconstructed phylogeny that differs from those currently published (Navajas-Pérez et al. 2005; Schuster et al. 2015) and has tested the placement and monophyly of its circumscribed subgenera. This work builds on those previous studies by providing an increased taxon sampling density, which has resulted in a more comprehensive reconstruction of the evolutionary history of Rumex and a more thorough examination of the stability of the subgeneric system. This work has provided an early outline of the evolution of reproductive systems in Rumex, suggesting an ordered plasticity and transitions from synoecy to dioecy to dioecy with heteromorphic sex chromosomes. Additionally, this work suggests a possible reversal from a dioecious condition. Future directions in Rumex research include the identification and application of nuclear markers that will allow for a more robust phylogeny, particularly with respect to the placement of Emex. Additionally, future genomic studies will serve to elucidate the evolution of the sex chromosomes and sex determining regions in Rumex.

Acknowledgements

This study was largely funded by award NSF-HRD #1601031 to J.M. Burke. The authors would like to thank staff at the following herbaria for facilitating access to specimens for sampling: K, NY, OSC, RAB and US. Special thanks to Spencer Barrett and Joanna Rifkin for access to cultivated Rumex material. We also thank Daniel Atha for providing us with a record of his Rumex collections and facilitating access to silica-dried material. Special thanks to Mr. Ibrahim El Hafid for his assistance with transportation during the Morocco expedition. We also thank Ms. Maria Ramos for her assistance with plant cultivation at the Howard University greenhouse.

References

  • Burke JM, Sanchez A, Kron KA, Luckow MA (2010) Placing the woody tropical genera of Polygonaceae: A hypothesis of character evolution and phylogeny. American Journal of Botany 97(8): 1377–1390. https://doi.org/10.3732/ajb.1000022
  • Cunado N, Navajas-Pérez R, de la Herrán R, Rejón CR, Rejón MR, Santos JL, Garrido-Ramos MA (2007) The evolution of sex chromosomes in the genus Rumex (Polygonaceae): Identification of a new species with heteromorphic sex chromosomes. Chromosome Research 15(7): 825–833. https://doi.org/10.1007/s10577-007-1166-6
  • Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T (2020) ModelTest-NG: A new scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution 37(1): 291–294. https://doi.org/10.1093/molbev/msz189
  • Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32(5): 1792–1797. https://doi.org/10.1093/nar/gkh340
  • Fazekas AJ, Burgess KS, Kesanakurti PR, Graham SW, Newmaster SG, Husband BC, Percy DM, Hajibabaei M, Barrett SC (2008) Multiple multilocus DNA barcodes from the plastid genome discriminate plant species equally well. PLoS ONE 3(7): e2802. https://doi.org/10.1371/journal.pone.0002802
  • Grant KD (2022) A new phylogeny of Rumex (Polygonaceae) adds evolutionary context to the diversity of reproductive systems present in the genus. Dryad, Dataset.
  • Hough J, Hollister JD, Wang W, Barrett SC, Wright SI (2014) Genetic degeneration of old and young Y chromosomes in the flowering plant Rumex hastatulus. Proceedings of the National Academy of Sciences of the United States of America 111(21): 7713–7718. https://doi.org/10.1073/pnas.1319227111
  • Löve Á (1957) Sex determination in Rumex. Proceedings of the Genetic Society of Canada 2: 31–36.
  • Löve Á, Löve D (1948) Chromosome numbers of northern plant species. Department of Agriculture, Reykjavik, University Institute of Applied Sciences.
  • Maddison WP (2005) Mesquite: a modular system for evolutionary analysis. Version 1.06. http://mesquiteproject.org [accessed 30.11.2019]
  • Mariotti B, Navajas-Pérez R, Lozano R, Parker JS, De La Herrán R, Rejón CR, Rejon MR, Garrido-Ramos M, Jamilena M (2006) Cloning and characterization of dispersed repetitive DNA derived from microdissected sex chromosomes of Rumex acetosa. Genome 49(2): 114–121. https://doi.org/10.1139/g05-089
  • Mariotti B, Manzano S, Kejnovský E, Vyskot B, Jamilena M (2009) Accumulation of Y-specific satellite DNAs during the evolution of Rumex acetosa sex chromosomes. Molecular Genetics and Genomics 281(3): 249. https://doi.org/10.1007/s00438-008-0405-7
  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), Institute of Electrical and Electronics Engineers, New Orleans, 1–8. http://doi.org/10.1109/GCE.2010.5676129
  • Mosyakin A (2005) Rumex. In: Flora of North America Editorial Committee (Eds) Flora of North America North of Mexico, Volume 5. Oxford University Press, New York, 1–690.
  • Navajas-Pérez R, de la Herrán R, González GL, Jamilena M, Lozano R, Rejón CR, Rejón MR, Garrido-Ramos MA (2005) The evolution of reproductive systems and sex-determining mechanisms within Rumex (Polygonaceae) inferred from nuclear and chloroplastidial sequence data. Molecular Biology and Evolution 22(9): 1929–1939. https://doi.org/10.1093/molbev/msi186
  • Rechinger KH (1933) Vorarbeiten zu einer Monographie der Gattung Rumex, III. Die Süd-und zentralamerikanischen Arten der Gattung Rumex. Arkiv för botanik 26A(3): 1–58.
  • Rechinger KH (1937) The North American species of Rumex. Field Museum of Natural History, 1–151.
  • Rechinger KH (1939) Polygonaceae. In: Hegi G, Hanser C (Eds) Illustrierte flora von Mittel – Europa. Verlag, Munich, 352–436.
  • Rechinger KH (1954a) Monograph of the genus Rumex in Africa: vorarbeiten zu einer Monographie der Gattung Rumex VIII. Gleerup, 1–114.
  • Rechinger KH (1954b) Beiträge zur kenntnis von Rumex XII: Some new American species of Rumex. Leaflets of Western Botany 7: 133–135.
  • Rechinger KH (1990) Rumex subgen. Rumex sect. Axillares (Polygonaceae) in South America. Plant Systematics and Evolution 172: 151–192. https://doi.org/10.1007/BF00937805
  • Ronquist FM, Teslenko P, Van Der Mark DL, Ayres A, Darling S, Hohna B, Larget L, Liu MA, Suchard J, Huelsenbeck P (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029
  • Sanchez A, Schuster TM, Kron KA (2009) A Large‐Scale Phylogeny of Polygonaceae Based on Molecular Data. International Journal of Plant Sciences 170(8): 1044–1055. https://doi.org/10.1086/605121
  • Sanchez A, Schuster TM, Burke JM, Kron KA (2011) Taxonomy of Polygonoideae (Polygonaceae): A new tribal classification. Taxon 60(1): 151–160. https://doi.org/10.1002/tax.601013
  • Schuster TM, Setaro SD, Kron KA (2013) Age estimates for the buckwheat family Polygonaceae based on sequence data calibrated by fossils and with a focus on the Amphi-Pacific Muehlenbeckia. PLoS ONE 8(4): e61261. https://doi.org/10.1371/journal.pone.0061261
  • Schuster TM, Reveal JL, Bayly MJ, Kron KA (2015) An updated molecular phylogeny of Polygonoideae (Polygonaceae): Relationships of Oxygonum, Pteroxygonum, and Rumex, and a new circumscription of Koenigia. Taxon 64(6): 1188–1208. https://doi.org/10.12705/646.5
  • Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal Of Botany 92(1): 142–166. https://doi.org/10.3732/ajb.92.1.142
  • Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. American Journal Of Botany 94(3): 275–288. https://doi.org/10.3732/ajb.94.3.275
  • Shibata F, Hizume M, Kuroki Y (1999) Chromosome painting of Y chromosomes and isolation of a Y chromosome-specific repetitive sequence in the dioecious plant Rumex acetosa. Chromosoma 108(4): 266–270. https://doi.org/10.1007/s004120050377
  • Shibata F, Hizume M, Kuroki Y (2000) Differentiation and the polymorphic nature of the Y chromosomes revealed by repetitive sequences in the dioecious plant, Rumex acetosa. Chromosome Research 8(3): 229–236. https://doi.org/10.1023/A:1009252913344
  • Thiers B (2019) Index Herbariorum: The William & Lynda Steere Herbarium, The New York Botanical Garden (updated continuously). http://sweetgum.nybg.org/science/ih/ [accessed 30.11.2019]
  • Wagner WL, Sohmer SH, Herbst DR (1999) Manual of the flowering plants of Hawai’i. University of Hawaii Press, 1–1952.
  • Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD Thesis, The University of Texas at Austin, Austin, Texas.

Appendix A1. List of taxa sampled and vouchers specimens

Abbreviations of herbaria where the voucher is housed are listed after the collection number. Sequences can be found on the Dryad database: https://doi.org/10.5061/dryad.69p8cz8zs

For sequences that we did not generate, accession information is given as found on GenBank.

GenBank sequences used for this study:

rbcL: Rumex pamiricus Rech. f. – JF944139.1, Rumex sibiricus Hulten- KC483892.1

trnH-psbA: Rumex pamiricus- JN047053.1

Table A1.

DNA Sequences Generated for this Study.

Scientific name Voucher
Emex australis Steinh. P.C. Zietsma 4053, NY
Emex spinosa (L.) Campd. Schuhwerk 90/328, NY
Emex spinosa (L.) Campd. J.M. Burke 302, HUDC
Persicaria virginiana (L.) Gaertn. J.M. Burke s.n., BH
Rheum alexandrae Batalin Cultivated Material, HUDC
Rheum emodii Wall. Cultivated Material, HUDC
Rheum officinale Baill. Cultivated Material, HUDC
Rheum palmatum var. taguticaum L. Cultivated Material, HUDC
Rheum rhabarbarum L. Cultivated Material, HUDC
Rheum nobile Hook. f. & Thomson Pradham 820581, BH
Rumex abyssinicus Jacq. J.M. Burke 251, HUDC
Rumex acetosa L. K.D. Grant s.n., HUDC
Rumex acetosella L. R. Brand 1336, NY
Rumex acetosella L. D.E. Atha 10521, NY
Rumex acetosella L. K.D. Grant s.n., HUDC
Rumex acetosella L. J.M. Burke 309, HUDC
Rumex albescens Hillebr. Lorence 5224, K
Rumex albescens Hillebr. Wood 14959, US
Rumex alpinus L. Larsen 20708, US
Rumex alpinus L. D.E. Atha 5114, NY
Rumex altissimus Alph, Wood Shultz 8717, US
Rumex altissimus Alph. Wood D.E. Atha 10857, NY
Rumex alveolatus Los.-Losinsk. Rechinger 48318, US
Rumex amurensis F. Schmidt ex Maxim. Barrett Lilan22p
Rumex aquaticus L. Elias 7251, US
Rumex arcticus Trautv. Shetler 4560, US
Rumex arifolius All. K. Deguchi 4023, NY
Rumex bequaertii De Wild. Germishuizen 3447, US
Rumex berlandieri Meisn. Thieret 17178, US
Rumex brachypodus Rech. f. J.M. Burke 312, HUDC
Rumex brasiliensis Link R. Wasum 1655, NY
Rumex brownii Campd. Wilson 10250, NY
Rumex brownii Campd. Wilson 10250, US
Rumex bucephalophorus L. Barrett 17RBTA5
Rumex bucephalophorus L. J.M. Burke 293, HUDC
Rumex bucephalophorus L. J.M. Burke 301, HUDC
Rumex bucephalophorus L. J.M. Burke 304, HUDC
Rumex chrysocarpus Moris D.E. Atha 13012, NY
Rumex conglomeratus Murray D.E. Atha 10045, NY
Rumex conglomeratus Murray J.M. Burke 271, HUDC
Rumex conglomeratus Murray J.M. Burke 298, HUDC
Rumex conglomeratus Murray J.M. Burke 299, HUDC
Rumex crispus L. J.M. Burke 268, HUDC
Rumex cuneifolius Campd. J.C. Solomon 13044, US
Rumex cyprius Murb. Kocher B-273, US
Rumex densiflorus Osterh. Pinkava P12626, US
Rumex dentatus L. D.G. Kelch 07.328, OSC
Rumex giganteus Aiton K. Thorne 6736, NY
Rumex giganteus Aiton Canfield 1304, US
Rumex graminifolius Gerogi ex Lamb. Petrosky 1811, US
Rumex hastatulus Baldwin D.E. Atha 10503, NY
Rumex hastatus D. Don MacArthur 1291, US
Rumex hastatus D. Don Barrett s.n.
Rumex hymenosepalus Torr. Cultivated material, HUDC
Rumex hymenosepalus Torr. A. Tiehm 15727, OSC
Rumex induratus Bioss. et Reut. M.W. Chase 925, K
Rumex induratus Bioss. et Reut. Barrett s.n.
Rumex induratus Bioss. et Reut. J.M. Burke 310, HUDC
Rumex intermedius DC. Rainha 5270, US
Rumex japonicus Houtt. Bai-Zhang 4049, US
Rumex kerneri Borbás Barta 2004-390, US
Rumex lanceolatus Thunb. H.J. Venter 10295, NY
Rumex longifolius DC. D. E. Atha 8858, NY
Rumex lunaria L. NR. 8879, NY
Rumex lunaria L. Barrett 17RLLM1
Rumex lunaria L. Barrett 17RLTF1
Rumex maritimus L. Shiu Ying Hu 13127, US
Rumex mexicanus Meisn. D.E. Breedlove 13305, US
Rumex microcarpus Campd. Barrett MJ-P40 (Seed)
Rumex nepalensis Spreng. J.M. Burke 248, HUDC
Rumex nervosus Vahl J.M. Burke 252, HUDC
Rumex obtusifolius L. J.M. Burke s.n., BH
Rumex obtusifolius L. J.M. Burke 270, HUDC
Rumex orbiculatus A. Gray Ruee 43716, US
Rumex orbiculatus A. Gray D.E. Atha et al. 8883/2010, NY
Rumex pallidus Bigelow D.E. Atha 13922, NY
Rumex palustris Sm. J.M. Burke 306, HUDC
Rumex papilio Coss. & Balansa, S.L. Jury 13659, K
Rumex papilio Coss. & Balansa J.M. Burke 303, HUDC
Rumex patientia L. D.E. Atha 10674, NY
Rumex paucifolius Nutt. Barrett 17RpCOT3.2
Rumex paucifolius Nutt. Barrett 17RpCMC15.2
Rumex peruanus Rech. f. V. Quipuscoa 1349, NY
Rumex pictus Forssk. Barrett 17Rp.AR1
Rumex pulcher L. J.M. Burke 294, HUDC
Rumex pulcher L. J.M. Burke 295, HUDC
Rumex pulcher L. J.M. Burke 296, HUDC
Rumex rothschildianus Aarons. ex Evenari Barrett 17Rrs3.2
Rumex sagittatus Thunb. Strobach B55575, US
Rumex sagittatus Thunb. H.J. Venter 9995, NY
Rumex salicifolius Weinm. W. Wood s.n., OSC
Rumex sanguineus L. J.M. Burke 316., HUDC
Rumex scutatus L. Barrett s.n.
Rumex skottsbergii O.Deg. & I.Deg. Degener 35050, US
Rumex spiralis Small. D.E. Atha 9727, NY
Rumex stenophyllus Ledeb. D.E. Atha 11389, NY
Rumex stenophyllus Ledeb. R.L. McGregor 40643, OSC
Rumex tianschanicus Losinsk. Barrett SH1-A-2007454
Rumex thyrsiflorus Fingerh. Ollegard 261, US
Rumex thyrsiflorus Fingerh. Elias 7282, US
Rumex thyrsoides Desf. J.M. Burke 305, HUDC
Rumex thyrsoides Desf. J.M. Burke 313, HUDC
Rumex thyrsoides Desf. J.M. Burke 307, HUDC
Rumex tuberosus L. S. Omar et al. 52591, K
Rumex tuberosus subsp. nov J.M. Burke 308, HUDC
Rumex usambarensis (Dammer) Dammer Ellemann 889, NY
Rumex venosus Pursh. R.E. Brainerd 428, OSC
Rumex vesicarius L. Brummit 15271, US

Supplementary material

Supplementary material 1 

Aligned Data Matrix

Kirstie D. Grant

Data type: FASTA

Explanation note: Aligned sequence file.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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