Key message
MAGIC populations present novel challenges and opportunities in crops due to their complex pedigree structure. They offer great potential both for dissecting genomic structure and for ...improving breeding populations.
The past decade has seen the rise of multiparental populations as a study design offering great advantages for genetic studies in plants. The genetic diversity of multiple parents, recombined over several generations, generates a genetic resource population with large phenotypic diversity suitable for high-resolution trait mapping. While there are many variations on the general design, this review focuses on populations where the parents have all been inter-mated, typically termed Multi-parent Advanced Generation Intercrosses (MAGIC). Such populations have already been created in model animals and plants, and are emerging in many crop species. However, there has been little consideration of the full range of factors which create novel challenges for design and analysis in these populations. We will present brief descriptions of large MAGIC crop studies currently in progress to motivate discussion of population construction, efficient experimental design, and genetic analysis in these populations. In addition, we will highlight some recent achievements and discuss the opportunities and advantages to exploit the unique structure of these resources post-QTL analysis for gene discovery.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
Domesticated crops experience strong human-mediated selection aimed at developing high-yielding varieties adapted to local conditions. To detect regions of the wheat genome subject to selection ...during improvement, we developed a high-throughput array to interrogate 9,000 gene-associated single-nucleotide polymorphisms (SNP) in a worldwide sample of 2,994 accessions of hexaploid wheat including landraces and modern cultivars. Using a SNP-based diversity map we characterized the impact of crop improvement on genomic and geographic patterns of genetic diversity. We found evidence of a small population bottleneck and extensive use of ancestral variation often traceable to founders of cultivars from diverse geographic regions. Analyzing genetic differentiation among populations and the extent of haplotype sharing, we identified allelic variants subjected to selection during improvement Selective sweeps were found around genes involved in the regulation of flowering time and phenology. An introgression of a wild relative-derived gene conferring resistance to a fungal pathogen was detected by haplotype-based analysis. Comparing selective sweeps identified in different populations, we show that selection likely acts on distinct targets or multiple functionally equivalent alleles in different portions of the geographic range of wheat. The majority of the selected alleles were present at low frequency in local populations, suggesting either weak selection pressure or temporal variation in the targets of directional selection during breeding probably associated with changing agricultural practices or environmental conditions. The developed SNP chip and map of genetic variation provide a resource for advancing wheat breeding and supporting future population genomic and genome-wide association studies in wheat.
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BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
Rhizosheaths comprise soil that adheres to plant roots and, in some species, are indicative of root hair length. In this study, the genetics of rhizosheath size in wheat was investigated by screening ...the progeny of multiparent advanced generation intercrosses (MAGIC). Two MAGIC populations were screened for rhizosheath size using a high throughput method. One MAGIC population was developed from intercrosses between four parents (4-way) and the other from intercrosses between eight parents (8-way). Transgressive segregation for rhizosheath size was observed in both the 4-way and 8-way MAGIC populations. A quantitative trait loci (QTL) analysis of the 4-way population identified six major loci located on chromosomes 2B, 4D, 5A, 5B, 6A, and 7A together accounting for 42% of the variation in rhizosheath size. Rhizosheath size was strongly correlated with root hair length and was robust across different soil types in the absence of chemical constraints. Rhizosheath size in the MAGIC populations was a reliable surrogate for root hair length and, therefore, the QTL identified probably control root hair elongation. Members of the basic helix-loop-helix family of transcription factors have previously been identified to regulate root hair length in Arabidopsis and rice. Since several wheat members of the basic helix-loop-helix family of genes are located within or near the QTL, these genes are candidates for controlling the long root hair trait. The QTL for rhizosheath size identified in this study provides the opportunity to implement marker-assisted selection to increase root hair length for improved phosphate acquisition in wheat.
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BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
The dissection of gene-trait associations and its translation into practice through plant breeding is a central aspect of modern plant biology. The identification of genes underlying simply inherited ...traits has been very successful. However, the identification of gene-trait associations for complex (multi-genic) traits in crop plants with large, often polyploid genomes has been limited by the absence of appropriate genetic resources that allow quantitative trait loci (QTL) and causal genes to be identified and localised. There has also been a tendency for genetic resources to be developed in germplasm not directly relevant to the breeding community limiting effective implementation. In this review, we discuss approaches to mapping genes and the development of Multi-parent Advanced Generation Inter-cross (MAGIC) populations derived from breeder-relevant germplasm as a platform for a new generation of gene-trait analysis in crop species.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UL, UM, UPCLJ, UPUK
Summary
We present the first results from a novel multiparent advanced generation inter‐cross (MAGIC) population derived from four elite wheat cultivars. The large size of this MAGIC population (1579 ...progeny), its diverse genetic composition and high levels of recombination all contribute to its value as a genetic resource. Applications of this resource include interrogation of the wheat genome and the analysis of gene–trait association in agronomically important wheat phenotypes. Here, we report the utilization of a MAGIC population for the first time for linkage map construction. We have constructed a linkage map with 1162 DArT, single nucleotide polymorphism and simple sequence repeat markers distributed across all 21 chromosomes. We benchmark this map against a high‐density DArT consensus map created by integrating more than 100 biparental populations. The linkage map forms the basis for further exploration of the genetic architecture within the population, including characterization of linkage disequilibrium, founder contribution and inclusion of an alien introgression into the genetic map. Finally, we demonstrate the application of the resource for quantitative trait loci mapping using the complex traits plant height and hectolitre weight as a proof of principle.
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BFBNIB, DOBA, FZAB, GIS, IJS, IZUM, KILJ, NLZOH, NUK, OILJ, PILJ, PNG, SAZU, SBCE, SBMB, UILJ, UKNU, UL, UM, UPUK
BACKGROUND: Measuring grain characteristics is an integral component of cereal breeding and research into genetic control of seed development. Measures such as thousand grain weight are fast, but do ...not give an indication of variation within a sample. Other methods exist for detailed analysis of grain size, but are generally costly and very low throughput. Grain colour analysis is generally difficult to perform with accuracy, and existing methods are expensive and involved. RESULTS: We have developed a software method to measure grain size and colour from images captured with consumer level flatbed scanners, in a robust, standardised way. The accuracy and precision of the method have been demonstrated through screening wheat and Brachypodium distachyon populations for variation in size and colour. CONCLUSION: By using GrainScan, cheap and fast measurement of grain colour and size will enable plant research programs to gain deeper understanding of material, where limited or no information is currently available.
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IZUM, KILJ, NUK, PILJ, PNG, SAZU, UL, UM, UPUK
Next-generation sequencing technologies provide new opportunities to identify the genetic components responsible for trait variation. However, in species with large polyploid genomes, such as bread ...wheat, the ability to rapidly identify genes underlying quantitative trait loci (QTL) remains non-trivial. To overcome this, we introduce a novel pipeline that analyses, by RNA-sequencing, multiple near-isogenic lines segregating for a targeted QTL.
We use this approach to characterize a major and widely utilized seed dormancy QTL located on chromosome 4AL. It exploits the power and mapping resolution afforded by large multi-parent mapping populations, whilst reducing complexity by using multi-allelic contrasts at the targeted QTL region. Our approach identifies two adjacent candidate genes within the QTL region belonging to the ABA-induced Wheat Plasma Membrane 19 family. One of them, PM19-A1, is highly expressed during grain maturation in dormant genotypes. The second, PM19-A2, shows changes in sequence causing several amino acid alterations between dormant and non-dormant genotypes. We confirm that PM19 genes are positive regulators of seed dormancy.
The efficient identification of these strong candidates demonstrates the utility of our transcriptomic pipeline for rapid QTL to gene mapping. By using this approach we are able to provide a comprehensive genetic analysis of the major source of grain dormancy in wheat. Further analysis across a diverse panel of bread and durum wheats indicates that this important dormancy QTL predates hexaploid wheat. The use of these genes by wheat breeders could assist in the elimination of pre-harvest sprouting in wheat.
The number of rachis nodes (spikelets) on a wheat spike is a component of grain yield that correlates with flowering time. The genetic basis regulating flowering in cereals is well understood, but ...there are reports that flowering time can be modified at a high frequency by selective breeding, suggesting that it may be regulated by both epigenetic and genetic mechanisms. We investigated the role of DNA methylation in regulating spikelet number and flowering time by treating a semi‐spring wheat with the demethylating agent, Zebularine. Three lines with a heritable increase in spikelet number were identified. The molecular basis for increased spikelet number was not determined in 2 lines, but the phenotype showed non‐Mendelian inheritance, suggesting that it could have an epigenetic basis. In the remaining line, the increased spikelet phenotype behaved as a Mendelian recessive trait and late flowering was associated with a deletion encompassing the floral promoter, FT‐B1. Deletion of FT‐B1 delayed the transition to reproductive growth, extended the duration of spike development, and increased spikelet number under different temperature regimes and photoperiod. Transiently disrupting DNA methylation can generate novel flowering behaviour in wheat, but these changes may not be sufficiently stable for use in breeding programs.
We investigated whether the demethylating agent Zebularine could be used as a tool to generate novel phenotypes for wheat breeding programs. Zebularine treatment delayed flowering and increased spikelet number in three plants of a semi‐spring wheat variety. The increased spikelet phenotype in two of these lines showed non‐Mendelian inheritance suggesting that it could be associated with a transient loss of DNA methylation, whereas in the third line, this phenotype was conditioned by a stably inherited recessive trait associated with deletion of FT‐B1, a major gene controlling flowering time in wheat. Loss of FT‐B1 resulted in increased spikelet number under all environmental conditions tested; the robust nature of this phenotype suggests that this deletion could be a valuable resource for breeding wheat with increased yield.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Identification of alleles towards the selection for improved seedling vigour is a key objective of many wheat breeding programmes. A multiparent advanced generation intercross (MAGIC) population ...developed from four commercial spring wheat cultivars (cvv. Baxter, Chara, Westonia and Yitpi) and containing ca. 1000 F₂‐derived, F₆:₇ RILs was assessed at two contrasting soil temperatures (12 and 20 °C) for shoot length and coleoptile characteristics length and thickness. Narrow‐sense heritabilities were high for coleoptile and shoot length (h² = 0.68–0.70), indicating a strong genetic basis for the differences among progeny. Genotypic variation was large, and distributions of genotype means were approximately Gaussian with evidence for transgressive segregation for all traits. A number of significant QTL were identified for all early growth traits, and these were commonly repeatable across the different soil temperatures. The largest negative effects on coleoptile lengths were associated with Rht‐B1b (−8.2%) and Rht‐D1b (−10.9%) dwarfing genes varying in the population. Reduction in coleoptile length with either gene was particularly large at the warmer soil temperature. Other large QTL for coleoptile length were identified on chromosomes 1A, 2B, 4A, 5A and 6B, but these were relatively smaller than allelic effects at the Rht‐B1 and Rht‐D1 loci. A large coleoptile length effect allele (a = 5.3 mm at 12 °C) was identified on chromosome 1AS despite the relatively shorter coleoptile length of the donor Yitpi. Strong, positive genetic correlations for coleoptile and shoot lengths (rg = 0.85–0.90) support the co‐location of QTL for these traits and suggest a common physiological basis for both. The multiparent population has enabled the identification of promising shoot and coleoptile QTL despite the potential for the confounding of large effect dwarfing gene alleles present in the commercial parents. The incidence of these alleles in commercial wheat breeding programmes should facilitate their ready implementation in selection of varieties with improved establishment and early growth.
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BFBNIB, DOBA, FZAB, GIS, IJS, IZUM, KILJ, NLZOH, NUK, OILJ, PILJ, PNG, SAZU, SBCE, SBMB, UILJ, UKNU, UL, UM, UPUK
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