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Kanadys W, Baranska A, Blaszczuk A, et al. Evaluation of clinical meaningfulness of red clover (Trifolium pratense L.) extract to relieve hot flashes and menopausal symptoms in peri- and post-menopausal women: a systematic review and meta-analysis of randomized controlled trials. Nutrients. 2021;13(4):1258. doi:10.3390%2Fnu13041258

Thorup AC, Lambert MN, Strom Kahr H, et al. Intake of novel red clover supplementation for 12 weeks improves bone status in healthy menopausal women. Evidenced-Based Complementary and Alternative Medicine. 2015;2015:689138. doi:10.1155%2F2015%2F689138

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Karimpour-Reihan S, Firuzei E, Khosravi M, et al. Coagulation disorder following red clover (Trifolium pratense) misuse: a case report. Advanced Journal of Emergency Medicine. 2018;2(2):e20. doi:10.22114%2Fajem.v0i0.30

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White clover (Trifolium repens L.) is a temperate forage legume with an allotetraploid genome (2n=4=32) estimated at 1093 Mb. Several linkage maps of various sizes, marker sources and completeness are available, however, no integrated map and marker set has explored consistency of linkage analysis among unrelated mapping populations. Such integrative analysis requires tools for homoeologue matching among populations. Development of these tools provides for a consistent framework map of the white clover genome, and facilitates in silico alignment with the model forage legume, Medicago truncatula.

This is the first report of integration of independent linkage maps in white clover, and adds to the literature on methyl filtered GeneThresher-derived microsatellite (simple sequence repeat; SSR) markers for linkage mapping. Gene-targeted SSR markers were discovered in a GeneThresher (TrGT) methyl-filtered database of 364,539 sequences, which yielded 15,647 SSR arrays. Primers were designed for 4,038 arrays and of these, 465 TrGT-SSR markers were used for parental consensus genetic linkage analysis in an F1 mapping population (MP2). This was merged with an EST-SSR consensus genetic map of an independent population (MP1), using markers to match homoeologues and develop a multi-population integrated map of the white clover genome. This integrated map (IM) includes 1109 loci based on 804 SSRs over 1274 cM, covering 97% of the genome at a moderate density of one locus per 1.2 cM. Eighteen candidate genes and one morphological marker were also placed on the IM. Despite being derived from disparate populations and marker sources, the component maps and the derived IM had consistent representations of the white clover genome for marker order and genetic length. In silico analysis at an E-value threshold of 1e-20 revealed substantial co-linearity with the Medicago truncatula genome, and indicates a translocation between T. repens groups 2 and 6 relative to M. truncatula.

This integrated genetic linkage analysis provides a consistent and comprehensive linkage analysis of the white clover genome, with alignment to a model forage legume. Associated marker locus information, particularly the homoeologue-specific markers, offers a new resource for forage legume research to enable genetic analysis and improvement of this forage and grassland species.

White clover (Trifolium repens L.) is a temperate perennial forage legume widely used in pastoral systems. The species produces high quality herbage, hosts Rhizobia bacteria that transform atmospheric nitrogen into plant available forms, exhibits compatibility and persistence in mixed species pastures, and contributes to soil quality [5, 6]. Propagated sexually by seed and asexually by stolons, it is an outcrossing disomic tetraploid (2n=4=32) with abundant sequence polymorphism and highly heterogeneous populations [7, 8]. White clover progenitors are putatively identified as the diploid species T. occidentale and T. pallescens[9, 10]. The white clover genome is moderately compact, estimated at 1093 Mb (1C; [11]), with high sequence similarity in orthologous genic regions within homoeologous pairs [12].

Minor agricultural species, such as white clover, often lag in the development of genomics resources. A range of marker platforms is now available, and the choice among systems is influenced by genome structure, reproductive biology of the species, and consideration of development costs, scale and system efficiency. Targeting marker discovery to specific genome fractions can influence the effectiveness of a marker resource. Markers in low copy number genic regions, such as expressed sequence tag (EST)-derived sources are more likely to be associated with polymorphisms conferring trait effects and are preferred in agricultural plants, however these markers generally exhibit reduced rates of polymorphism [13, 14]. Methylation-filtration targets genomic sequence surveys to genic regions, providing gene-rich marker discovery data [15]. As a marker development resource, these sequences share the gene-associated benefits of EST-derived sequence data and the higher polymorphism rate of genomic-derived sequence data. Methyl-filtered sequences are also free from bias created by enriching or screening genomic libraries for specific simple sequence repeat (SSR; microsatellite) motifs, or using expressed sequence data from specific tissues or plant growth stages.

Marker development from targeted sequence can identify polymorphism based on sequence identity (e.g. single nucleotide polymorphism, SNP) or length, such as SSR arrays. In the absence of reference genomes for white clover and progenitors, homoeologous sequence similarity in genic regions hinders development of an efficient SNP discovery process. This is predominantly due to a high proportion of putative SNP markers in silico arising from conflation of orthologous sequence within homoeologous pairs [16]. Reference sequence from progenitor species [9, 10] partially overcomes this limitation [17], however SNP discovery and utilisation in white clover remains a challenge.

The Trifolieae forage legume model Medicago truncatula, with links to the wider legume phyla community and other agricultural crops [33], is of primary interest in white clover comparative genetics. In silico referencing of white clover to M. truncatula has identified macrosyntenic relationships maintained between these two species [19, 34, 35], supported by evidence from mapped comparative markers [22]. This has led to the Medicago chromosomal nomenclature replacing the initial Trifolium nomenclature of Barrett et al. [20].

The objectives of this research were to: establish an integrated genetic linkage map of the white clover genome based on linkage analysis in two independent F1 mapping populations; develop candidate gene-targeted markers for traits of interest as a platform for functional markers and to aid genome alignment with other species; identify homoeologue-specific markers; document a comprehensive set of mapped white clover microsatellite markers; and enrich the in silico alignment between Trifolium repens and Medicago truncatula.

Although derived from unrelated populations and distinct marker sources, the linkage maps of MP2 (Additional file 3) and MP1 [20] revealed a similar view of the white clover genome in terms of shared marker order and linkage group size (Table 2). Improved map statistics were observed for MP2 (Table 2) and were a reflection of the 49% increase in marker loci and 39% increase in marker density relative to MP1.

The in silico alignment of the IM to assembly version 3.0 of the Medicago truncatula genome revealed 376 hits at an E-value threshold of 1e-20 for 822 T. repens mapped marker query sequences. Mean alignment span for the 376 hits was 242 bp with a mean E-value of 4.4e-22. There were similar values for ESTs and TrGT sequences. Inspection revealed 81% of the aligned sequences followed a linear pattern of macrosyntenic alignment with consistent coverage of M. truncatula hits across most of the T. repens genome (Figure 4). The remaining 19% were more widely scattered (Figure 4). The alignment supports relating the T. repens nomenclature of Barrett et al. [20] with M. truncatula (Mt) groups as follows: Mt-1 = E with 39 hits; Mt-3 = A with 49 hits; Mt-4 = D with 34 hits; Mt-5 = G with 53 hits; Mt-7 = C with 37 hits; and Mt-8 = B with 50 hits. Groups 3, 4, 5, 7, and 8 as presented in Barrett et al. [20] were inverted in T. repens relative to M. truncatula; in Figures 2, 4 and 3 and Additional file 3 they have been matched with the M. truncatula orientation. Relative to M. truncatula, there may be short inversions within white clover groups 1, 4 and 8; however these may be artefacts of constraints in linkage analysis or genome assembly.

This integrated map is anchored by gene-targeted SSR markers mined from a white clover GeneThresher (TrGT) genomic DNA sequence and from ESTs. EST-derived markers exhibit less polymorphism, but have a higher probability of being directly linked to a causative gene than genomic SSRs [3]. Repeat number in EST-SSRs is usually low and a predominance of trinucleotide motifs is explained by changes in other common motif lengths causing frame shifts disrupting coding sequence [3, 55]. The white clover EST-SSR source had a preponderance of trinucleotide motifs and a mode of four repeats per array [20], whereas the methyl-filtered TrGT source was predominately dinucleotides motifs, with a mode of eight repeats. Only 71% of EST-derived SSRs produced PCR products [20], compared with 86% [29] and 92% from array targeted white clover genomic libraries [27] and from TrGT-derived SSRs in this study. Intron presence may affect the efficiency of generating amplicons from expressed sequence sourced SSRs, as well as influencing the observed versus predicted amplicon size. Mean observed amplicon size of white clover EST-derived SSRs was 128% of the size predicted in silico[20], compared with 103% for TrGT-derived SSRs. Reduced amplification efficiency attributed to M13(-21) primer-based fluorophore addition [56] has been demonstrated [57, 58], suggesting that more than 92% of the TrGT-derived SSR primer pairs are viable. ff782bc1db