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The major clades of subgenus Trifolium. The area of the triangles is proportional to the number of species in each clade. Branch shading corresponds to life history. All species shown here are 2n D 16, except for T. lupinaster; T. gordejevii is uncounted.
Source publication
Trifolium, the clover genus, is one of the largest genera of the legume family. We conducted parsimony and Bayesian phylogenetic analyses based on nuclear ribosomal DNA internal transcribed spacer and chloroplast trnL intron sequences obtained from 218 of the ca. 255 species of Trifolium, representatives from 11 genera of the vicioid clade, and an...
Contexts in source publication
Context 1
... Trifolium (Fig. 3) has a paraphyletic grade at its base, comprising sect. Paramesus and Wve Eurasian perennials that we place in sect. Glycyrrhizum and sect. Lupinaster (Table 1). These Wve species are sometimes placed in two segregate genera (see Section 4.2.). There is strong support for a sister group relationship between sect. Lupinaster and the ...
Context 2
... at its base, comprising sect. Paramesus and Wve Eurasian perennials that we place in sect. Glycyrrhizum and sect. Lupinaster (Table 1). These Wve species are sometimes placed in two segregate genera (see Section 4.2.). There is strong support for a sister group relationship between sect. Lupinaster and the remaining Wve sections of the subgenus (Fig. 3). The monophyly of these Wve sections, and their inter-relationships, are well supported by the Bayesian analysis (PP 70.95) but most have <85% BP ...
Context 3
... formerly classiWed in sect. Lotoidea. This clade includes the economically important white clover, T. repens. Many relationships within this clade are resolved in the Bayesian analysis, but have BP values below 50%. Likewise, the sister-group relationship between this clade and the American clovers (sect. Involucrarium) has <50% BP, but PP D 0.99 (Fig. ...
Context 4
... to limited sampling of species diversity in other genera of the vicioid clade (Table 2), the ancestral life history for Trifo- lium cannot be inferred. The annual habit is the ancestral state reconstruction for subgenus Chronosemium (Fig. 2), while the ancestral state for subgenus Trifolium is equivocal (Fig. 3). Within this subgenus, the common ancestor of sects. Trifolium and Trichocephalum is inferred to be annual, while the common ancestor of the three other large sections is inferred to be peren- nial (Fig. 3). Within subgenus Chronosemium there is one change to the perennial habit involving two species (Fig. 2), and within sect. ...
Context 5
... habit is the ancestral state reconstruction for subgenus Chronosemium (Fig. 2), while the ancestral state for subgenus Trifolium is equivocal (Fig. 3). Within this subgenus, the common ancestor of sects. Trifolium and Trichocephalum is inferred to be annual, while the common ancestor of the three other large sections is inferred to be peren- nial (Fig. 3). Within subgenus Chronosemium there is one change to the perennial habit involving two species (Fig. 2), and within sect. Trifolium there are seven changes (Fig. 4). Five of these are autapomorphic, while the others involve clades of three and seven species, respectively. Among the sections with a perennial ancestral state, there are ...
Context 6
... , 1978. To maintain nomenclatural stability, we do not advocate this change, but propose that the hop clovers should be considered one of two subgenera of Trifolium. Following this classiWcation, the remaining species of Trifolium are placed in subgenus Trifo- lium. We further propose recognizing eight of its clades as sections (Table 1 and Fig. 3). The designation of this infra- generic classiWcation is greatly facilitated by the thorough nomenclatural work of Hendrych (1988). The larger clades could be further divided into subsections, but this is prema- ture pending more intensive sampling and better phyloge- netic resolution at this taxonomic level. With few exceptions, the ...
Context 7
... we can be fairly conWdent that the ancestor of subgenus Chronosemium was an annual (Fig. 2), the ances- tral state of subgenus Trifolium is uncertain (Fig. 3). Reso- lution of the polytomy between the annual sect. Paramesus and the perennial sect. Glycyrrhizum should clarify this. Within subgenus Trifolium, two sections ( Trifolium and Trichocephalum) share an annual ancestry, while three sec- tions (Vesicastrum, Trifoliastrum, and Involucrarium) share a perennial ancestry. Across the genus, ...
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Citations
... White clover (Trifolium repens) is a perennial allotetraploid (2n = 4x = 32) legume formed from the interspecific hybridisation of two diploid (2n = 2x = 16) progenitors, and is found globally in temperate and some tropical regions where it has significant agronomic use as a forage legume (Alencar et al., 2024;Griffiths et al., 2019). The extant descendants of white clover progenitors (EDprogenitors) are T. occidentale, a species restricted to the coastal regions of western Europe (Coombe, 1961) and T. pallescens, which grows in European alpine regions above 1800 m (Ellison et al., 2006;Raffl et al., 2008;Williams et al., 2012). White clover is a recent hybrid, estimated to have originated during the depths of the last glaciation~20,000 years ago (Figure 1a), and is an example of niche expansion facilitated by allopolyploidy as it is widespread in temperate climates (Griffiths et al., 2019). ...
... This individual provides insight into how a clover neopolyploid may respond to frost stress compared to the EDprogenitors and whether there was an ecological advantage over either of the progenitors. TO and TP were included as they are the EDprogenitors of white clover (Ellison et al., 2006;Williams et al., 2012), and show how the coastal-restricted TO and the alpine-adapted TP react to frost stress and provide comparators for response of the white clovers and neopolyploid. ...
Allotetraploid white clover ( Trifolium repens ) formed during the last glaciation through hybridisation of two European diploid progenitors from restricted niches: one coastal, the other alpine. Here, we examine which hybridisation‐derived molecular events may have underpinned white clover's postglacial niche expansion. We compared the transcriptomic frost responses of white clovers (an inbred line and an alpine‐adapted ecotype), extant descendants of its progenitor species and a resynthesised white clover neopolyploid to identify genes that were exclusively frost‐induced in the alpine progenitor and its derived subgenomes. From these analyses we identified galactinol synthase, the rate‐limiting enzyme in biosynthesis of the cryoprotectant raffinose, and found that the extant descendants of the alpine progenitor as well as the neopolyploid white clover rapidly accumulated significantly more galactinol and raffinose than the coastal progenitor under cold stress. The frost‐induced galactinol synthase expression and rapid raffinose accumulation derived from the alpine progenitor likely provided an advantage during early postglacial colonisation for white clover compared to its coastal progenitor.
... Accordingly, the search for rhizobial isolates with high tolerance to stress conditions may be a way of improving legume yields, especially in more adverse climate and soil conditions. Clovers (Trifolium spp.) represent a large genus of the Fabaceae family encompassing ~ 250 different species from different geographical regions (Europe, North and South America, Australia, and Africa) [40][41][42] . The red clover (Trifolium pratense L.) is one of the most widely cultivated forage plants in Europe, North America, and Australia 43,44 . ...
... trifolii strains derived from three clover species (red clover, white clover, and alsike clover) from Northern Norway also showed a lower diversity of symbiotic genes than that in our strains. A total of 12 nodEF genotypes and 6 nifDK genotypes were identified among 75 strains 41 . Taken together, the degree of symbiotic diversity of rhizobial populations depends on several factors such as the legume host species, place of their origin, and climate conditions as well as symbiotic genes and techniques used. ...
Red clover (Trifolium pratense L.) is a forage legume cultivated worldwide. This plant is capable of establishing a nitrogen-fixing symbiosis with Rhizobium leguminosarum symbiovar trifolii strains. To date, no comparative analysis of the symbiotic properties and heterogeneity of T. pratense microsymbionts derived from two distinct geographic regions has been performed. In this study, the symbiotic properties of strains originating from the subpolar and temperate climate zones in a wide range of temperatures (10–25 °C) have been characterized. Our results indicate that all the studied T. pratense microsymbionts from two geographic regions were highly efficient in host plant nodulation and nitrogen fixation in a wide range of temperatures. However, some differences between the populations and between the strains within the individual population examined were observed. Based on the nodC and nifH sequences, the symbiotic diversity of the strains was estimated. In general, 13 alleles for nodC and for nifH were identified. Moreover, 21 and 61 polymorphic sites in the nodC and nifH sequences were found, respectively, indicating that the latter gene shows higher heterogeneity than the former one. Among the nodC and nifH alleles, three genotypes (I–III) were the most frequent, whereas the other alleles (IV–XIII) proved to be unique for the individual strains. Based on the nodC and nifH allele types, 20 nodC-nifH genotypes were identified. Among them, the most frequent were three genotypes marked as A (6 strains), B (5 strains), and C (3 strains). Type A was exclusively found in the temperate strains, whereas types B and C were identified in the subpolar strains. The remaining 17 genotypes were found in single strains. In conclusion, our data indicate that R. leguminosarum sv. trifolii strains derived from two climatic zones show a high diversity with respect to the symbiotic efficiency and heterogeneity. However, some of the R. leguminosarum sv. trifolii strains exhibit very good symbiotic potential in the wide range of the temperatures tested; hence, they may be used in the future for improvement of legume crop production.
... We annotated 96,293 protein coding genes in the primary haplotig, which is slightly more than double the number of genes in the diploid genome of the related legume Medicago truncatula (44,295); this nding is consistent with white clover's tetraploid genome. A total of 61,352 of the annotated genes were successfully mapped by BLAST against the NCBI RefSeq database and functionally annotated with the GO database. ...
... The genus Trifolium is characterized by extensive chromosome number variation between species and occasional polyploid speciation events [44]. In our genomic comparisons with the closely related legume Medicago truncatula, white clover shows the most conserved chromosome structure of the three Trifolium species with reference genomes, the other two of which are diploid; T. pratense (2n = 14) and T. subterraneum (2n = 16) each possess a minimum of 2-3 chromosomal rearrangements in a majority of their chromosomes (Fig. 2C). ...
Background
White clover (Trifolium repens) is a globally important perennial forage legume. This species also serves as an eco-evolutionary model system for studying within-species chemical defense variation; it features a well-studied polymorphism for cyanogenesis (HCN release following tissue damage), with higher frequencies of cyanogenic plants favored in warmer locations worldwide. Using a newly-generated haplotype-resolved genome and two other long-read assemblies, we tested the hypothesis that copy number variants (CNVs) at cyanogenesis genes play a role in the ability of white clover to rapidly adapt to local environments. We also examined questions on subgenome evolution in this recently evolved allotetraploid species and on chromosomal rearrangements in the broader IRLC legume clade.
Results
Integration of PacBio HiFi, Omni-C, Illumina and linkage map data yielded the first completely de novo genome assembly for white clover (created without a priori sequence assignment to subgenomes). We find that white clover has undergone extensive transposon diversification since its origin but otherwise shows highly conserved genome organization and composition with its diploid progenitors; unlike some other clover species, its chromosomal structure is conserved with other IRLC legumes. We further find extensive evidence of CNVs at the major cyanogenesis loci; these contribute to quantitative variation in the cyanogenic phenotype and to local adaptation across wild North American populations.
Conclusions
This study is among the first, to our knowledge, to document the role of CNVs in local adaptation in a plant species, and it highlights the value of pan-genome data for identifying contributions of structural variants to adaptation in nature.
... Trifolium is one of the most important genera of the Fabaceae family, both in terms of agricultural use and the number of species (about 300) (Baskin and Baskin, 2004). The Mediterranean region is very rich in Trifolium species (clovers), where these species are widely spread in natural areas (Ellison et al., 2006). Clovers have excellent potential as a weed suppressor, in addition to other advantages, like nitrogen fixation and the reduction of pests and diseases in several crops (Den Hollander et al., 2007). ...
This research was carried out to evaluate the effect of (1) different methods of breaking seed dormancy (physical and chemical scarification, high temperature, hot water and after-ripening), and (2) environmental factors (temperature, salinity and water stress) on seed germination of Trifolium angustifolium , T. arvense , T. fragiferum , T. fucatum , T. repens , T. subterraneum and Trifolium sp. All experiments were conducted in the Seed Research Laboratory of Gorgan University of Agricultural Sciences and Natural Resources, Iran, in 2021. All the examined clover species were dormant after harvest, with little germination. Mechanical scarification with sandpaper or sulphuric acid resulted in more than 88 and 52% germination, respectively. Seeds were able to germinate between 5 and 35°C, but the highest germination (≥ 98% on average) occurred at 20°C. Fluctuating temperature regimes were more efficient in improving the germination than constant temperatures. Seeds of clover species, in addition to having a hard seed coat, have a non-deep physiological dormancy. Fresh seeds showed a high sensitivity to water stress compared with after-ripened seeds. However, relative resistance to salinity stress was observed. The results obtained in this research can be used to develop effective sowing strategies and support the successful establishment of these clover species.
... The ITS and some restriction fragment analysis data have been used for the phylogeny of the genus Trifolium (Watson et al, (2000;Ellison et al, 2006) and by Badr et al (unpublished data). The parsimony and Bayesian phylogenetic analyses based on the ITS of nrDNA and chloroplast trnL intron (Ellison et al, 2006) confirmed the monophyly of Trifolium, and propose a new infra-generic classification of the genus based on the phylogenetic results. ...
... The ITS and some restriction fragment analysis data have been used for the phylogeny of the genus Trifolium (Watson et al, (2000;Ellison et al, 2006) and by Badr et al (unpublished data). The parsimony and Bayesian phylogenetic analyses based on the ITS of nrDNA and chloroplast trnL intron (Ellison et al, 2006) confirmed the monophyly of Trifolium, and propose a new infra-generic classification of the genus based on the phylogenetic results. Incongruence between the nrDNA and cpDNA results suggests six cases of apparent hybrid speciation, and identified the putative progenitors of the allopolyploids T. dubium, a widespread weed, and T. repens, the most commonly cultivated clover species. ...
... The results are consistent with a Mediterranean origin of the genus, probably in the Early Miocene. A single origin of all North and South American species is hypothesized, while the species of sub-Saharan Africa may originate from three separate dispersal events (Ellison et al, 2006). Trifolium section Trifolium based on ITS sequence, using Trofolium alpinum and Trifolium aureum as out groups. ...
Plant taxonomy and systematics, particularly classification is essentially based on the morphological criteria of plants. Criteria derived from other plant features such as anatomy, chromosomes, and the characteristics of pollens, embryos, and seeds have provided important information for the taxonomic delimitation of many plant groups. However, the use of these criteria as sources of taxonomic information has been gradually overtaken by the modern use of molecular data derived from DNA and proteins. These data because of the sequential transfer of genetic code from DNA to proteins provide the means for elucidating the genetic basis for all biological diversity and a universal standard for comparing all forms of life. Characters derived from proteins have been obtained by four approaches i.e. serological comparisons, native or denatured protein electrophoresis, allozymes, and isozymes polymorphism, also revealed by electrophoresis and amino acid sequencing. However, characters derived from proteins are gradually replaced by more powerful and more informative DNA data. Systematic information from DNA has been obtained by several approaches; the most common are the restriction fragment analysis, restriction fragment length polymorphism (RFLP), nucleotide sequencing of chloroplast and nuclear genes and the analysis of DNA amplification products produced by using polymerase chain reaction (PCR) by the random amplification of polymorphic DNA (RAPD), inter simple sequence repeats (ISSR) and amplified fragment length polymorphism (AFLP). In this article, I comment on the contribution of the different types of taxonomic information and describe the sources of molecular data particularly the methods used to obtain evidence from the DNA properties. The implications of the DNA-based information on the systematics of selected groups of plants are also briefly described. The article also includes recommendations for the application of DNA data in systematic studies.
... The genetic resources of these indigenous underutilized species are in danger of being rapidly destroyed because of the deterioration of traditional agricultural practices, changes in traditional eating patterns, and the introduction and adaptation of high yielding crops, even though fenugreek is thought to be a vital component of minor crops [8]. In fact, the availability of fenugreek germplasm is low or almost scanty in gene banks [9,10]. The fact that fenugreek accessions (land races) are impacted by climate change or the shrinking amount of arable land is a major cause for concern. ...
A research work on genetic divergence, analysis was estimated in 75 genotypes of fenugreek (Trigonella foenum-graecum L.) grown in an Augmented Block Design during Rabi season of 2019-20 at Main Experiment Station of Department of Vegetable Science Acharya Narendra Deva University of Agriculture and Technology, Ayodhya. The objective of this study was to characterize morphological differences and yield related traits among 75 fenugreek accessions. Genetic diversity among 75 fenugreek genotypes (Trigonella foenum-graecum L.) was assessed. The estimation of genetic diversity among tested genotypes was highly significant, which got grouped into 8 clusters with cluster VI comprising maximum genotypes. Maximum intra-cluster distance (31.23) was observed in cluster V followed by cluster IV (15.51). Similarly maximum inter cluster distance was recorded between the cluster V and VIII (111.88) followed by cluster III and VIII (111.81) respectively. Although maximum cluster means for seed yield traits was recorded for cluster V and III respectively, suggesting a wide range of diversity for most of the economic traits that would enable breeder to identify the genotypes with suitable traits to be used in direct selection and also in improvement programme for broadening the genetic base. 75 accession showed distinguished variation in the dendrogram for all the studied parameters.
... Clover plays a vital role in major agroecological zones as one of the most significant forage crops, and it serves as a crucial component for sustainable intensification of livestock farming systems [1]. It contains a high protein content and does not require considerable nitrogen fertilizer input unlike other forage crops that belong to the family gramineae [2]. ...
... Clover belongs to one of the largest genera Trifolium in the family Fabaceae and consists of ca. 255 species [1]. It occurs naturally in subtropical and temperate regions of both the Southern and Northern Hemispheres. ...
Citation: Areej, A.; Nawaz, H.; Aslam, I.; Danial, M.; Qayyum, Z.; Rasool, U.A.; Asif, J.; Khalid, A.; Serfraz, S.; Saleem, F.; et al.
... Clover plays a vital role in major agroecological zones as one of the most significant forage crops, and it serves as a crucial component for sustainable intensification of livestock farming systems [1]. It contains a high protein content and does not require considerable nitrogen fertilizer input unlike other forage crops that belong to the family gramineae [2]. ...
... Clover belongs to one of the largest genera Trifolium in the family Fabaceae and consists of ca. 255 species [1]. It occurs naturally in subtropical and temperate regions of both the Southern and Northern Hemispheres. ...
Crop wild relatives contain a greater variety of phenotypic and genotypic diversity compared to their domesticated counterparts. Trifolium crop species have limited genetic diversity to cope with biotic and abiotic stresses due to artificial selection for consumer preferences. Here, we investigated the distribution and evolution of nucleotide-binding site leucine-rich repeat receptor (NLR) genes in the genus of Trifolium with the objective to identify reference NLR genes. We identified 412, 350, 306, 389 and 241 NLR genes were identified from Trifolium. subterraneum, T. pratense, T. occidentale, subgenome-A of T. repens and subgenome-B of T. repens, respectively. Phylogenetic and clustering analysis reveals seven sub-groups in genus Trifolium. Specific subgroups such as G4-CNL, CCG10-CNL and TIR-CNL show distinct duplication patterns in specific species, which suggests subgroup duplications that are the hallmarks of their divergent evolution. Furthermore, our results strongly suggest the overall expansion of NLR repertoire in T. subterraneum is due to gene duplication events and birth of gene families after speciation. Moreover, the NLRome of the allopolyploid species T. repens has evolved asymmetrically, with the subgenome -A showing expansion, while the subgenome-B underwent contraction. These findings provide crucial background data for comprehending NLR evolution in the Fabaceae family and offer a more comprehensive analysis of NLR genes as disease resistance genes.
... Tribe: Trifolieae Section: Vesicaria (T. fragiferum is the lectotype for this Section) Genus: Trifolium Species: fragiferum Ellison et al. (2006), in a phylogenetic study of the Trifolium genus, suggested a new classification, with T. fragiferum placed in section Vesicastrum within subgenus Trifolium of the genus Trifolium. ...
Strawberry clover (Trifolium fragiferum L.) is periodically raised as an alternative perennial pasture legume for temperate regions of Australia. Its tolerance of waterlogging is widely known, yet its ability to persist through periods of soil moisture deficit is often understated. Other desirable characteristics include its stoloniferous growth habit and tolerance of mildly saline conditions. Only four strawberry clover cultivars have been registered in Australia, and the most popular, cv. Palestine, is a direct introduction, released in 1938 and first certified in 1951. Furthermore, strawberry clover’s distribution has largely been confined to niche environments, particularly waterlogged and saline areas. This paper reviews the taxonomy and breeding system, morphology, distribution and ecology, and subsequent transfer of strawberry clover to Australia. It reviews and maps the suitability of strawberry clover for perennial pasture systems in the medium–-high rainfall and irrigated temperate zones of Australia, with reference to future climates. The paper also highlights the breeding focus, commercialisation and marketing required to supersede cv. Palestine and lists the germplasm available in the Australian Pastures Genebank, with origins. We conclude that, although strawberry clover is unlikely to become a dominant perennial pasture legume species in Australia, it could be used in a wider range of environments than just those affected by salinity and/or waterlogging stress.
... Trifolium Linnaeus (1753: 764) is one of the largest genera of the legume family with ca. 255 species; that is an extremely difficult genus (Zohary & Heller 1984, Ellison et al. 2006, Ahmed et al. 2021, as observed in the Mediterranean Basin especially in hotspot areas also in other plant genera, such as Carex, Centaurea, Geranium, Limonium, etc. (Wagensommer et al. 2014, Wagensommer et al. 2016, Brullo & Erben 2016, Wagensommer & Venanzoni 2021, Garmendia et al. 2022. The three primary diversity centers for the genus Trifolium have located approximately in Turkey (Mediterranean center), Ethiopia (African center), and northern California, USA (American center) (Zohary & Heller 1984). ...
... This branch of science, advancing day by day, examines the different DNA structures in living things in detail. Genus Trifolium is also an important study focus at this point, but it is difficult to say that the results obtained in the studies fully confirm each other (Taylor et al. 1979, Bennett 2000, Watson et al. 2000, Wojciechowski 2003, Ellison et al. 2006, Rizza et al. 2007, Abate 2017. ...
Trifolium elazizense, a new species of Trifolium sect. Trifolium from East Anatolia in Turkey is described. It grows in subalpine regions with steep slopes and shallow soil at high altitudes. The new species is morphologically close to T. longidentatum and T. kurdistanicum, and can be considered a member of the new subsect. Stipulia. Trifolium elazizense is characterized by hairy stipules, the throat of calyx closed by callus hairs, inflorescences without bracts, obviously unequal calyx teeth, longest tooth 3-nerved, others 1–3 nerved.
