Publications by authors named "Susanne Dreisigacker"

66 Publications

Linkage disequilibrium patterns, population structure and diversity analysis in a worldwide durum wheat collection including Argentinian genotypes.

BMC Genomics 2021 Apr 5;22(1):233. Epub 2021 Apr 5.

Centro de Recursos Naturales Renovables de la Zona Semiárida (CERZOS), Departamento de Agronomía, Universidad Nacional del Sur (UNS)-CONICET, Bahía Blanca, Argentina.

Background: Durum wheat (Triticum turgidum L. ssp. durum Desf. Husn) is the main staple crop used to make pasta products worldwide. Under the current climate change scenarios, genetic variability within a crop plays a crucial role in the successful release of new varieties with high yields and wide crop adaptation. In this study we evaluated a durum wheat collection consisting of 197 genotypes that mainly comprised a historical set of Argentinian germplasm but also included worldwide accessions.

Results: We assessed the genetic diversity, population structure and linkage disequilibrium (LD) patterns in this collection using a 35 K SNP array. The level of polymorphism was considered, taking account of the frequent and rare allelic variants. A total of 1547 polymorphic SNPs was located within annotated genes. Genetic diversity in the germplasm collection increased slightly from 1915 to 2010. However, a reduction in genetic diversity using SNPs with rare allelic variants was observed after 1979. However, larger numbers of rare private alleles were observed in the 2000-2009 period, indicating that a high reservoir of rare alleles is still present among the recent germplasm in a very low frequency. The percentage of pairwise loci in LD in the durum genome was low (13.4%) in our collection. Overall LD and the high (r > 0.7) or complete (r = 1) LD presented different patterns in the chromosomes. The LD increased over three main breeding periods (1915-1979, 1980-1999 and 2000-2020).

Conclusions: Our results suggest that breeding and selection have impacted differently on the A and B genomes, particularly on chromosome 6A and 2A. The collection was structured in five sub-populations and modern Argentinian accessions (cluster Q4) which were clearly differentiated. Our study contributes to the understanding of the complexity of Argentinian durum wheat germplasm and to derive future breeding strategies enhancing the use of genetic diversity in a more efficient and targeted way.
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http://dx.doi.org/10.1186/s12864-021-07519-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8022437PMC
April 2021

Genome-Wide Association Study of Tan Spot Resistance in a Hexaploid Wheat Collection From Kazakhstan.

Front Genet 2020 11;11:581214. Epub 2021 Jan 11.

Global Wheat Program, International Maize and Wheat Improvement Center (CIMMYT), Texcoco, Mexico.

Tan spot, caused by , is a serious foliar disease of wheat in Kazakhstan with reported yield losses as high as 50% during epidemic years. Here, we report the evaluation of a collection of 191 hexaploid spring and winter wheat lines for tan spot resistance and its underlying genetic architecture using genome-wide association study (GWAS). Our wheat collection comprised candidate varieties from Kazakhstan, Russia, and CIMMYT. It was genotyped using the DArTseq technology and phenotyped for resistance to tan spot at seedling and adult plant stages in Kazakhstan. DArTseq SNPs revealed high genetic diversity (average polymorphic information content = 0.33) in the panel and genome-wide linkage disequilibrium decay at 22 Mb (threshold = 0.1). Principal component analysis revealed a clear separation of Eurasian germplasm from CIMMYT and IWWIP lines. GWAS identified 34 marker-trait associations (MTA) for resistance to tan spot and the amount of phenotypic variation explained by these MTA ranged from 4% to 13.7%. Our results suggest the existence of novel valuable resistant alleles on chromosomes 3BS, and 5DL and 6AL for resistance to Race 1 and Race 5, respectively, in addition to known genes and On chromosome 6AL, a genomic region spanning 3 Mb was identified conferring resistance to both Race 1 and Race 5. Epistatic interaction of associated loci was revealed on chromosomes 1B, 5B, 7B, 5A, and 6A contributing to additional variation of 3.2-11.7%. Twenty-five lines with the best allele combinations of SNPs associated with resistance to both races have been identified as candidates for future variety release and breeding. The results of the present study will be further validated in other independent genetic backgrounds to be able to use markers in breeding.
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http://dx.doi.org/10.3389/fgene.2020.581214DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7831376PMC
January 2021

Genomic resources in plant breeding for sustainable agriculture.

J Plant Physiol 2021 Feb 17;257:153351. Epub 2020 Dec 17.

Center of Excellence in Genomics & Systems Biology, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Hyderabad, India. Electronic address:

Climate change during the last 40 years has had a serious impact on agriculture and threatens global food and nutritional security. From over half a million plant species, cereals and legumes are the most important for food and nutritional security. Although systematic plant breeding has a relatively short history, conventional breeding coupled with advances in technology and crop management strategies has increased crop yields by 56 % globally between 1965-85, referred to as the Green Revolution. Nevertheless, increased demand for food, feed, fiber, and fuel necessitates the need to break existing yield barriers in many crop plants. In the first decade of the 21st century we witnessed rapid discovery, transformative technological development and declining costs of genomics technologies. In the second decade, the field turned towards making sense of the vast amount of genomic information and subsequently moved towards accurately predicting gene-to-phenotype associations and tailoring plants for climate resilience and global food security. In this review we focus on genomic resources, genome and germplasm sequencing, sequencing-based trait mapping, and genomics-assisted breeding approaches aimed at developing biotic stress resistant, abiotic stress tolerant and high nutrition varieties in six major cereals (rice, maize, wheat, barley, sorghum and pearl millet), and six major legumes (soybean, groundnut, cowpea, common bean, chickpea and pigeonpea). We further provide a perspective and way forward to use genomic breeding approaches including marker-assisted selection, marker-assisted backcrossing, haplotype based breeding and genomic prediction approaches coupled with machine learning and artificial intelligence, to speed breeding approaches. The overall goal is to accelerate genetic gains and deliver climate resilient and high nutrition crop varieties for sustainable agriculture.
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http://dx.doi.org/10.1016/j.jplph.2020.153351DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7903322PMC
February 2021

Genome-Wide Association Mapping and Genomic Prediction of Anther Extrusion in CIMMYT Hybrid Wheat Breeding Program via Modeling Pedigree, Genomic Relationship, and Interaction With the Environment.

Front Genet 2020 8;11:586687. Epub 2020 Dec 8.

Texas A&M University, College Station, TX, United States.

Anther extrusion (AE) is the most important male floral trait for hybrid wheat seed production. AE is a complex quantitative trait that is difficult to phenotype reliably in field experiments not only due to high genotype-by-environment effects but also due to the short expression window in the field condition. In this study, we conducted a genome-wide association scan (GWAS) and explored the possibility of applying genomic prediction (GP) for AE in the CIMMYT hybrid wheat breeding program. An elite set of male lines ( = 603) were phenotype for anther count (AC) and anther visual score (VS) across three field experiments in 2017-2019 and genotyped with the 20K Infinitum is elect SNP array. GWAS produced five marker trait associations with small effects. For GP, the main effects of lines (L), environment (E), genomic (G) and pedigree relationships (A), and their interaction effects with environments were used to develop seven statistical models of incremental complexity. The base model used only L and E, whereas the most complex model included L, E, G, A, and G × E and A × E. These models were evaluated in three cross-validation scenarios (CV0, CV1, and CV2). In cross-validation CV0, data from two environments were used to predict an untested environment; in random cross-validation CV1, the test set was never evaluated in any environment; and in CV2, the genotypes in the test set were evaluated in only a subset of environments. The prediction accuracies ranged from -0.03 to 0.74 for AC and -0.01 to 0.54 for VS across different models and CV schemes. For both traits, the highest prediction accuracies with low variance were observed in CV2, and inclusion of the interaction effects increased prediction accuracy for AC only. In CV0, the prediction accuracy was 0.73 and 0.45 for AC and VS, respectively, indicating the high reliability of across environment prediction. Genomic prediction appears to be a very reliable tool for AE in hybrid wheat breeding. Moreover, high prediction accuracy in CV0 demonstrates the possibility of implementing genomic selection across breeding cycles in related germplasm, aiding the rapid breeding cycle.
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http://dx.doi.org/10.3389/fgene.2020.586687DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7755068PMC
December 2020

Haplotype-Based, Genome-Wide Association Study Reveals Stable Genomic Regions for Grain Yield in CIMMYT Spring Bread Wheat.

Front Genet 2020 3;11:589490. Epub 2020 Dec 3.

International Maize and Wheat Improvement Center (CIMMYT), Texcoco, Mexico.

We untangled key regions of the genetic architecture of grain yield (GY) in CIMMYT spring bread wheat by conducting a haplotype-based, genome-wide association study (GWAS), together with an investigation of epistatic interactions using seven large sets of elite yield trials (EYTs) consisting of a total of 6,461 advanced breeding lines. These lines were phenotyped under irrigated and stress environments in seven growing seasons (2011-2018) and genotyped with genotyping-by-sequencing markers. Genome-wide 519 haplotype blocks were constructed, using a linkage disequilibrium-based approach covering 14,036 Mb in the wheat genome. Haplotype-based GWAS identified 7, 4, 10, and 15 stable (significant in three or more EYTs) associations in irrigated (I), mild drought (MD), severe drought (SD), and heat stress (HS) testing environments, respectively. Considering all EYTs and the four testing environments together, 30 stable associations were deciphered with seven hotspots identified on chromosomes 1A, 1B, 2B, 4A, 5B, 6B, and 7B, where multiple haplotype blocks were associated with GY. Epistatic interactions contributed significantly to the genetic architecture of GY, explaining variation of 3.5-21.1%, 3.7-14.7%, 3.5-20.6%, and 4.4- 23.1% in I, MD, SD, and HS environments, respectively. Our results revealed the intricate genetic architecture of GY, controlled by both main and epistatic effects. The importance of these results for practical applications in the CIMMYT breeding program is discussed.
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http://dx.doi.org/10.3389/fgene.2020.589490DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7737720PMC
December 2020

The Effect of Photoperiod Genes and Flowering Time on Yield and Yield Stability in Durum Wheat.

Plants (Basel) 2020 Dec 7;9(12). Epub 2020 Dec 7.

IRTA (Institute for Food and Agricultural Research and Technology), Sustainable Field Crops Program, 25198 Lleida, Spain.

This study analysed the effect of flowering time as influenced by photoperiod sensitivity genes on yield and yield stability in durum wheat. Twenty-three spring genotypes harbouring different allele combinations at and were grown in 15 field experiments at three sites at latitudes from 41° to 19° N (Spain, Mexico-North and Mexico-South). Low temperature and solar radiation before flowering and long day length during grain-filling characteristic for the Spanish site resulted in high grain number/m (GN) and yield (GY), while a moderate GN combined with high solar radiation during grain-filling at Mexico-North led to heavier grains. Allele combination GS100-/ reduced the flowering time up to nine days when compared with /. Differences in flowering time caused by / allele combinations did not affect yield. Combinations GS105-/ and / resulted in the highest GN, linked to spikelets/spike, which was higher in GS105-/ due to more grains/spikelet. Flowering time caused by had a minor effect on GN, spikes/m and grains/spike, but late flowering resulted in reduced grain weight and GY. Allele combinations harbouring alleles conferring a similar photoperiod sensitivity response at and resulted in greater yield stability than combinations that carry alleles conferring a different response. Allele combination GS100-/ was the most suitable in terms of yield and yield stability of durum wheat cultivated under irrigation within the studied latitudes.
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http://dx.doi.org/10.3390/plants9121723DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7762236PMC
December 2020

Genome-based prediction of multiple wheat quality traits in multiple years.

Plant Genome 2020 11 25;13(3):e20034. Epub 2020 Jul 25.

Department of Agronomy, Kansas State University, 2004 Throckmorton Plant Science Center, Manhattan, KS, 66506, USA.

Wheat quality improvement is an important objective in all wheat breeding programs. However, due to the cost, time and quantity of seed required, wheat quality is typically analyzed only in the last stages of the breeding cycle on a limited number of samples. The use of genomic prediction could greatly help to select for wheat quality more efficiently by reducing the cost and time required for this analysis. Here were evaluated the prediction performances of 13 wheat quality traits under two multi-trait models (Bayesian multi-trait multi-environment [BMTME] and multi-trait ridge regression [MTR]) using five data sets of wheat lines evaluated in the field during two consecutive years. Lines in the second year (testing) were predicted using the quality information obtained in the first year (training). For most quality traits were found moderate to high prediction accuracies, suggesting that the use of genomic selection could be feasible. The best predictions were obtained with the BMTME model in all traits and the worst with the MTR model. The best predictions with the BMTME model under the mean arctangent absolute percentage error (MAAPE) were for test weight across the five data sets, whereas the worst predictions were for the alveograph trait ALVPL. In contrast, under Pearson's correlation, the best predictions depended on the data set. The results obtained suggest that the BMTME model should be preferred for multi-trait prediction analyses. This model allows to obtain not only the correlation among traits, but also the correlation among environments, helping to increase the prediction accuracy.
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http://dx.doi.org/10.1002/tpg2.20034DOI Listing
November 2020

Adult Plant Slow Rusting Genes Confer High Levels of Resistance to Rusts in Bread Wheat Cultivars From Mexico.

Front Plant Sci 2020 14;11:824. Epub 2020 Jul 14.

CSIRO Agriculture and Food, Canberra, ACT, Australia.

Rust diseases continuously threaten global wheat production: stem rust, leaf rust, and yellow rust caused by f. sp. , , and f. sp. , respectively. Recent studies indicated that the average losses from all these three rusts reached up to 15.04 million tons per year, which is equivalent to an annual average loss of around US $2.9 billion per year. The major focus of Mexican and worldwide breeding programs is the release of rust resistant cultivars, as this is considered the best option for controlling rust diseases. In Mexico, the emphasis has been placed on genes that confer partial resistance in the adult plant stage and against a broad spectrum of rust races since the 1970s. In this study, a set of the first-generation tall varieties developed and released in the 1940s and 1950s, the first semi-dwarfs, and other releases in Mexico, all of which showed different levels of rust resistance have been phenotyped for the three rust diseases and genotyped. Results of the molecular marker detection indicated that , , , and alone or in different gene combinations were present among the wheat cultivars. Flag leaf tip necrosis was present in all cultivars and most were positive for brown necrosis or Pseudo Black Chaff associated with the stem rust resistance complex. The phenotypic responses to the different rust infections indicate the presence of additional slow rusting and race-specific resistance genes. The study reveals the association of the slow rusting genes with durable resistance to the three rusts including Ug99 in cultivars bred before the green revolution such as Frontera, Supremo 211, Chapingo 48, Yaqui 50, Kentana 52, Bajio 52, Bajio 53, Yaqui 53, Chapingo 53, Yaktana Tardio 54, and Mayo 54 and their descendants after intercrossing and recombination. These slow rusting genes are the backbone of the resistance in the current Mexican germplasm.
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http://dx.doi.org/10.3389/fpls.2020.00824DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7371971PMC
July 2020

Disease Resistance Evaluation of Elite CIMMYT Wheat Lines Containing the Coupled and Genes.

Plant Dis 2020 Sep 13;104(9):2369-2376. Epub 2020 Jul 13.

International Maize and Wheat Improvement Center (CIMMYT), El Batan, Mexico.

Fusarium head blight (FHB) and stem rust are among the most devastating diseases of wheat worldwide. is the most widely utilized and the only isolated gene for FHB resistance, while is a durable stem rust resistance gene used in rust-prone areas. The two loci are closely linked on the short arm of chromosome 3B and the two genes are in repulsion phase among cultivars. With climate change and the shift in populations, it is imperative to develop wheat cultivars resistant to both diseases. The present study was dedicated to developing wheat germplasm combining and resistance alleles in the International Maize and Wheat Improvement Center (CIMMYT)'s elite cultivars' backgrounds. Four recombinant inbred lines (RILs) in Hartog background that have the resistant and alleles in coupled phase linkage were crossed with seven CIMMYT bread wheat lines, resulting in 208 lines. Molecular markers for both genes were employed in addition to the use of pseudo-black chaff (PBC) as a phenotypic marker for the selection of . At various stages of the selection process, progeny lines were assessed for FHB index, Fusarium damaged kernels (FDK), stem rust, and PBC expression as well as other diseases of interest (stripe rust and leaf spotting diseases). The 25 best lines were selected for CIMMYT's wheat breeding program. In addition to expressing resistance to FHB, most of these 25 lines have an acceptable level of resistance to other tested diseases. These lines will be useful for wheat breeding programs worldwide and potentially speed up the resistance breeding efforts against FHB and stem rust.
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http://dx.doi.org/10.1094/PDIS-02-20-0369-REDOI Listing
September 2020

Allelic Variation at the Vernalization Response () and Photoperiod Sensitivity () Genes and Their Association With the Development of Durum Wheat Landraces and Modern Cultivars.

Front Plant Sci 2020 23;11:838. Epub 2020 Jun 23.

Sustainable Field Crops Programme, Institute for Food and Agricultural Research and Technology (IRTA), Lleida, Spain.

Wheat adaptability to a wide range of environmental conditions is mostly determined by allelic diversity within genes controlling vernalization requirement () and photoperiod sensitivity (). We characterized a panel of 151 durum wheat Mediterranean landraces and 20 representative locally adapted modern cultivars for their allelic composition at and gene using diagnostic molecular markers and studied their association with the time needed to reach six growth stages under field conditions over 6 years. Compared with the more diverse and representative landrace collection, the set of modern cultivars were characterized by a reduction of 50% in the number of allelic variants at the and genes, and the high frequency of mutant alleles conferring photoperiod insensitivity at , which resulted on a shorter cycle length. played a greater role than in regulating crop development ( > ). The results suggest that mutations in the gene may have been the most important in establishing the spring growth habit of Mediterranean landraces and modern durum cultivars. The allele , found in 10 landraces, delayed development. The relative effects of single alleles on delaying the development of the landraces were = > > . Allele was present in all except two landraces and in all modern cultivars. The null allele at (a deletion first observed in the French bread wheat cultivar 'Capelle-Desprez') was found for the first time in durum wheat in the present study that identified it in 30 landraces from 13 Mediterranean countries. Allele () was detected in both germplasm types, while the allele () was found only in modern North American and Spanish cultivars. The relative effect of single alleles on extending phenological development was () > > () > (). Sixteen allelic combinations were found in landraces and six in modern cultivars, but only three were common to both panels. Differences in the number of days to reach anthesis were 10 days in landraces and 3 days in modern cultivars. Interactive effects between and genes were detected.
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http://dx.doi.org/10.3389/fpls.2020.00838DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7325763PMC
June 2020

Quantitative Trait Loci Mapping for Spot Blotch Resistance in Two Biparental Mapping Populations of Bread Wheat.

Phytopathology 2020 Dec 15;110(12):1980-1987. Epub 2020 Oct 15.

International Maize and Wheat Improvement Center (CIMMYT), Apdo. Postal 6-641, 06600 Mexico DF, Mexico.

Spot blotch (SB), caused by , is a major fungal disease of wheat in South Asia and South America. Two biparental mapping populations with 232 F progenies each were generated, with CIMMYT breeding lines CASCABEL and KATH as resistant parents and CIANO T79 as the common susceptible parent. The two populations were evaluated for field SB resistance in CIMMYT's Agua Fria station for three consecutive cropping seasons, with artificial inoculation. Genotyping was done with the DArTseq platform and approximately 1,500 high quality and nonredundant markers were used for quantitative trait loci (QTL) mapping. In both populations, a major QTL was found on chromosome 5A in the region, explaining phenotypic variations of 13.5 to 25.9%, which turned up to be less- or nonsignificant when days to heading and plant height were used as covariates in the analysis, implying a disease escape mechanism. Another major QTL was located on chromosome 5B in CASCABEL, accounting for 8.9 to 21.4% of phenotypic variation. Minor QTL were found on 4A and 4B in CASCABEL; 1B, 4B, and 4D in KATH; and 1B, 2B, and 4B in CIANO T79. Through an analysis of QTL projection onto the IWGSC Chinese Spring reference genome, the 5B QTL in CASCABEL was mapped in the region, delimited by the single nucleotide polymorphism marker and the simple sequence repeat marker , with a physical distance of about 14 Mb to the locus.
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http://dx.doi.org/10.1094/PHYTO-05-20-0197-RDOI Listing
December 2020

Development and validation of high-throughput and low-cost STARP assays for genes underpinning economically important traits in wheat.

Theor Appl Genet 2020 Aug 25;133(8):2431-2450. Epub 2020 May 25.

Institute of Crop Sciences, National Wheat Improvement Center, Chinese Academy of Agricultural Sciences (CAAS), 12 Zhongguancun South Street, Beijing, 100081, China.

Key Message: We developed and validated 56 gene-specific semi-thermal asymmetric reverse PCR (STARP) markers for 46 genes of important wheat quality, biotic and abiotic stress resistance, grain yield, and adaptation-related traits for marker-assisted selection in wheat breeding. Development of high-throughput, low-cost, gene-specific molecular markers is important for marker-assisted selection in wheat breeding. In this study, we developed 56 gene-specific semi-thermal asymmetric reverse PCR (STARP) markers for wheat quality, tolerance to biotic and abiotic stresses, grain yield, and adaptation-related traits. The STARP assays were validated by (1) comparison of the assays with corresponding diagnostic STS/CAPS markers on 40 diverse wheat cultivars and (2) characterization of allelic effects based on the phenotypic and genotypic data of three segregating populations and 305 diverse wheat accessions from China and 13 other countries. The STARP assays showed the advantages of high-throughput, accuracy, flexibility, simple assay design, low operational costs, and platform compatibility. The state-of-the-art assays of this study provide a robust and reliable molecular marker toolkit for wheat breeding programs.
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http://dx.doi.org/10.1007/s00122-020-03609-wDOI Listing
August 2020

Regularized selection indices for breeding value prediction using hyper-spectral image data.

Sci Rep 2020 05 18;10(1):8195. Epub 2020 May 18.

Department of Epidemiology and Biostatistics, Michigan State University, East Lansing, MI, USA.

High-throughput phenotyping (HTP) technologies can produce data on thousands of phenotypes per unit being monitored. These data can be used to breed for economically and environmentally relevant traits (e.g., drought tolerance); however, incorporating high-dimensional phenotypes in genetic analyses and in breeding schemes poses important statistical and computational challenges. To address this problem, we developed regularized selection indices; the methodology integrates techniques commonly used in high-dimensional phenotypic regressions (including penalization and rank-reduction approaches) into the selection index (SI) framework. Using extensive data from CIMMYT's (International Maize and Wheat Improvement Center) wheat breeding program we show that regularized SIs derived from hyper-spectral data offer consistently higher accuracy for grain yield than those achieved by standard SIs, and by vegetation indices commonly used to predict agronomic traits. Regularized SIs offer an effective approach to leverage HTP data that is routinely generated in agriculture; the methodology can also be used to conduct genetic studies using high-dimensional phenotypes that are often collected in humans and model organisms including body images and whole-genome gene expression profiles.
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http://dx.doi.org/10.1038/s41598-020-65011-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7235263PMC
May 2020

SNP markers for low molecular glutenin subunits (LMW-GSs) at the Glu-A3 and Glu-B3 loci in bread wheat.

PLoS One 2020 12;15(5):e0233056. Epub 2020 May 12.

Global Wheat Program, International Maize and Wheat Improvement Center (CIMMYT), Texcoco, Mexico.

The content and composition of seed storage proteins is largely responsible for wheat end-use quality. They mainly consist of polymeric glutenins and monomeric gliadins. According to their electrophoretic mobility, gliadins and glutenins are subdivided into several fractions. Glutenins are classified as high molecular weight or low molecular weight glutenin subunits (HMW-GSs and LMW-GSs, respectively). LMW-GSs are encoded by multigene families located at the orthologous Glu-3 loci. We designed a set of 16 single-nucleotide polymorphism (SNP) markers that are able to detect SDS-PAGE alleles at the Glu-A3 and Glu-B3 loci. The SNP markers captured the diversity of alleles in 88 international reference lines and 27 Mexican cultivars, when compared to SDS-PAGE and STS markers, however, showed a slightly larger percent of multiple alleles, mainly for Glu-B3. SNP markers were then used to determine the Glu-1 and Glu-3 allele composition in 54 CIMMYT historical lines and demonstrated to be useful tool for breeding programs to improve wheat end product properties.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0233056PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7217469PMC
July 2020

Incorporating Genome-Wide Association Mapping Results Into Genomic Prediction Models for Grain Yield and Yield Stability in CIMMYT Spring Bread Wheat.

Front Plant Sci 2020 4;11:197. Epub 2020 Mar 4.

Global Wheat Program, International Maize and Wheat Improvement Center, Texcoco, Mexico.

Untangling the genetic architecture of grain yield (GY) and yield stability is an important determining factor to optimize genomics-assisted selection strategies in wheat. We conducted in-depth investigation on the above using a large set of advanced bread wheat lines (4,302), which were genotyped with genotyping-by-sequencing markers and phenotyped under contrasting (irrigated and stress) environments. Haplotypes-based genome-wide-association study (GWAS) identified 58 associations with GY and 15 with superiority index (measure of stability). Sixteen associations with GY were "environment-specific" with two on chromosomes 3B and 6B with the large effects and 8 associations were consistent across environments and trials. For , 8 associations were from chromosomes 4B and 7B, indicating 'hot spot' regions for stability. Epistatic interactions contributed to an additional 5-9% variation on average. We further explored whether integrating consistent and robust associations identified in GWAS as fixed effects in prediction models improves prediction accuracy. For GY, the model accounting for the haplotype-based GWAS loci as fixed effects led to up to 9-10% increase in prediction accuracy, whereas for this approach did not provide any advantage. This is the first report of integrating genetic architecture of GY and yield stability into prediction models in wheat.
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http://dx.doi.org/10.3389/fpls.2020.00197DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7064468PMC
March 2020

Effect of allele combinations at loci on durum wheat grain filling at contrasting latitudes.

J Agron Crop Sci 2020 Feb 15;206(1):64-75. Epub 2019 Sep 15.

Sustainable Field Crops Programme Institute for Food and Agricultural Research and Technology (IRTA) Lleida Spain.

Flowering time is the most critical developmental stage in wheat, as it determines environmental conditions during grain filling. Thirty-five spring durum genotypes carrying all known allele variants at loci were evaluated in fully irrigated field experiments for three years at latitudes of 41°N (Spain), 27°N (northern Mexico) and 19°N (southern Mexico). Relationships between weight of central grains of main spikes () and thermal time from flowering to maturity were described by a logistic equation. Differences in flowering time between the allele combination causing the earliest (GS100/) and the latest () flowering were 7, 20 and 18 days in Spain, northern Mexico and southern Mexico, respectively. Flowering delay drastically reduced the mean grain filling rate () and at all sites. At autumn-sowing sites, an increase of 1°C in mean temperature during the first half of the grain filling period decreased by 5.2 mg per grain. At these sites, was strongly dependent on . At the spring-sowing site (southern Mexico), depended on both and grain filling duration. Our results suggest that incorporating the allele combinations GS100/ and GS105/ (alleles conferring photoperiod insensitivity) in newly released varieties can reduce the negative effects of climate change on grain filling at the studied latitudes.
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http://dx.doi.org/10.1111/jac.12363DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7006787PMC
February 2020

Four Consistent Loci Confer Adult Plant Resistance to Leaf Rust in the Durum Wheat Lines Heller#1 and Dunkler.

Phytopathology 2020 Apr 26;110(4):892-899. Epub 2020 Feb 26.

Huazhong Agricultural University, College of Plant Science & Technology, Wuhan City, Hubei Province 430070, People's Republic of China.

The durum wheat lines Heller#1 and Dunkler from the International Maize and Wheat Improvement Center Global Wheat Program showed moderate and stable adult plant resistance to leaf rust under high disease pressure over field environments in northwestern Mexico. Leaf rust phenotyping was performed on two recombinant inbred line (RIL) populations derived from crosses of Heller#1 and Dunkler with the susceptible parent Atred#2, conducted under artificially induced epidemics in 2013, 2014, 2015, and 2016. The Atred#2 × Heller#1 and Atred#2 × Dunkler populations were genotyped by single nucleotide polymorphism (SNP) platforms and diversity arrays technology markers, respectively. Four leaf rust resistance quantitative trait loci were detected simultaneously in the two RIL populations: , , , and based on phenotypic data across all four crop seasons. They explained 11.7 to 46.8%, 7.2 to 26.1%, 8.4 to 24.1%, and 12.4 to 28.5%, respectively, of the phenotypic variation for leaf rust resistance in Atred#2 × Heller#1 and 16.3 to 56.6%, 6.7 to 15.7%, 4.1 to 10.1%, and 5.1 to 20.2% of the variation in the Atred#2 × Dunkler population. Only the resistance allele of was from the susceptible parent Atred#2, and resistance alleles at other loci came from the resistant parents Heller#1 and Dunkler. The SNP markers closely linked to and were converted to kompetitive allele specific PCR markers for use in marker-assisted selection to improve leaf rust resistance through crosses with Heller#1 and Dunkler sources.
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http://dx.doi.org/10.1094/PHYTO-09-19-0348-RDOI Listing
April 2020

Mapping of Genetic Loci Conferring Resistance to Leaf Rust From Three Globally Resistant Durum Wheat Sources.

Front Plant Sci 2019 8;10:1247. Epub 2019 Oct 8.

Department of Plant Sciences, Crop Development Centre, University of Saskatchewan, Saskatoon, SK, Canada.

Genetic resistance in the host plant is the most economical and environmentally friendly strategy for controlling wheat leaf rust, caused by Eriks. The durum wheat lines Gaza (Middle East), Arnacoris (France) and Saragolla (Italy) express high levels of resistance to the Mexican races of . Three recombinant inbred line (RIL) populations, derived from crosses of each of these resistance sources to the susceptible line ATRED #2, were evaluated for leaf rust reactions at CIMMYT's leaf rust nurseries in Mexico. Genetic analyses of host reactions suggested oligogenic control of resistance in all populations. The F RILs from each cross were genotyped using the Illumina iSelect 90K array, and high-density genetic maps were constructed for each population. Using composite interval mapping, a total of seven quantitative trait loci (QTL) that provide resistance to leaf rust were identified. Two QTL designated as and were identified on chromosome 6B in Gaza, which explained up to 78.5% and 21.3% of the observed leaf rust severity variance, respectively. A major QTL designated as was detected on the long arm of chromosome 7B in Arnacoris, which accounted for up to 65.9% of the disease severity variance. Arnacoris also carried a minor QTL on chromosome 1BL, designated as that explained up to 17.7% of the phenotypic variance. Three QTL conferred leaf rust resistance in Saragolla, namely , , and , which accounted for up to 42.3, 9.4, and 7.1% of the phenotypic variance, respectively. Markers flanking each QTL were physically mapped against the durum wheat reference sequence and candidate genes involved in disease resistance were identified within the QTL intervals. The QTL identified in this study and their closely linked markers are useful resources for gene pyramiding and breeding for durable leaf rust resistance in durum wheat.
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http://dx.doi.org/10.3389/fpls.2019.01247DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6792298PMC
October 2019

Validation of Candidate Gene-Based Markers and Identification of Novel Loci for Thousand-Grain Weight in Spring Bread Wheat.

Front Plant Sci 2019 26;10:1189. Epub 2019 Sep 26.

Department of Bioscience, CIMMYT, Texcoco, Mexico.

Increased thousand-grain weight (TGW) is an important breeding target for indirectly improving grain yield (GY). Fourteen reported candidate genes known to enhance TGW were evaluated in two independent and existing datasets of wheat at CIMMYT, the Elite Yield Trial (EYT) from 2015 to 2016 (EYT2015-16) and the Wheat Association Mapping Initiative (WAMI) panel, to study their allele effects on TGW and to verify their suitability for marker-assisted selection. Of these, significant associations were detected for only one gene () in the EYT2015-16 and two genes ( and ) in WAMI. The reported favorable alleles of and genes decreased TGW in the datasets. A haplotype-based genome wide association study was implemented to identify the genetic determinants of TGW on a large set of CIMMYT germplasm (4,302 lines comprising five EYTs), which identified 15 haplotype blocks to be significantly associated with TGW. Four of them, identified on chromosomes 4A, 6A, and 7A, were associated with TGW in at least three EYTs. The locus on chromosome 6A (Hap-6A-13) had the largest effect on TGW and additionally GY with increases of up to 2.60 g and 258 kg/ha, respectively. Discovery of novel TGW loci described in our study expands the opportunities for developing diagnostic markers and for multi-gene pyramiding to derive new allele combinations for enhanced TGW and GY in CIMMYT wheat.
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http://dx.doi.org/10.3389/fpls.2019.01189DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6775465PMC
September 2019

Improving grain yield, stress resilience and quality of bread wheat using large-scale genomics.

Nat Genet 2019 10 23;51(10):1530-1539. Epub 2019 Sep 23.

International Maize And Wheat Improvement Center (CIMMYT), Texcoco, Mexico.

Bread wheat improvement using genomic tools is essential for accelerating trait genetic gains. Here we report the genomic predictabilities of 35 key traits and demonstrate the potential of genomic selection for wheat end-use quality. We also performed a large genome-wide association study that identified several significant marker-trait associations for 50 traits evaluated in South Asia, Africa and the Americas. Furthermore, we built a reference wheat genotype-phenotype map, explored allele frequency dynamics over time and fingerprinted 44,624 wheat lines for trait-associated markers, generating over 7.6 million data points, which together will provide a valuable resource to the wheat community for enhancing productivity and stress resilience.
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http://dx.doi.org/10.1038/s41588-019-0496-6DOI Listing
October 2019

Genetic Contribution of Synthetic Hexaploid Wheat to CIMMYT's Spring Bread Wheat Breeding Germplasm.

Sci Rep 2019 08 26;9(1):12355. Epub 2019 Aug 26.

Global Wheat Program, International Maize and Wheat Improvement Center (CIMMYT), Carretera México-Veracruz Km 45, El Batán, Texcoco, C.P., 56237, Mexico.

Synthetic hexaploid (SH) wheat (AABBD'D') is developed by artificially generating a fertile hybrid between tetraploid durum wheat (Triticum turgidum, AABB) and diploid wild goat grass (Aegilops tauschii, D'D'). Over three decades, the International Maize and Wheat Improvement Center (CIMMYT) has developed and utilized SH wheat to bridge gene transfer from Ae. tauschii and durum wheat to hexaploid bread wheat. This is a unique example of success utilizing wild relatives in mainstream breeding at large scale worldwide. Our study aimed to determine the genetic contribution of SH wheat to CIMMYT's global spring bread wheat breeding program. We estimated the theoretical and empirical contribution of D' to synthetic derivative lines using the ancestral pedigree and marker information using over 1,600 advanced lines and their parents. The average marker-estimated D' contribution was 17.5% with difference in genome segments suggesting application of differential selection pressure. The pedigree-based contribution was correlated with marker-based estimates without providing chromosome segment specific variation. Results from international yield trials showed that 20% of the lines were synthetic derived with an average D' contribution of 15.6%. Our results underline the importance of SH wheat in maintaining and enhancing genetic diversity and genetic gain over years and is important for development of a more targeted introgression strategy. The study provides retrospective view into development and utilization of SH in the CIMMYT Global Wheat Program.
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http://dx.doi.org/10.1038/s41598-019-47936-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6710277PMC
August 2019

Genetic diversity and linkage disequilibrium using SNP (KASP) and AFLP markers in a worldwide durum wheat (Triticum turgidum L. var durum) collection.

PLoS One 2019 28;14(6):e0218562. Epub 2019 Jun 28.

Centro de Recursos Naturales Renovables de la Zona Semiárida (CERZOS-CCT-CONICET Bahía Blanca) and Departamento de Agronomía, Universidad Nacional del Sur, Bahía Blanca, Argentina.

The aim of this work was to analyze the genetic diversity and linkage disequilibrium in a collection of 168 durum wheat accessions (Triticum turgidum L. var. durum) of different origins. Our collection was mainly composed of released and unreleased Argentinian germplasm, with additional genotypes from Italy, Chile, France, CIMMYT, Cyprus, USA and WANA region. To this end, the entire collection was characterized with 85 Single Nucleotide Polymorphism (SNP) markers obtained by Kompetitive Allele Specific PCR (KASP), giving a heterozygosity (He) mean value of 0.183 and a coefficient of genetic differentiation (Gst) value of 0.139. A subset of 119 accessions was characterized with six Amplified Fragment Length Polymorphism (AFLP) primer combinations. A total of 181 polymorphic markers (125 AFLP and 56 SNP) amplified across this subset revealed He measures of 0.352 and 0.182, respectively. Of these, 134 were selected to estimate the genome-wide linkage disequilibrium obtaining low significant values (r2 = 0.11) in the subset, indicating its suitability for future genome-wide association studies (GWAS). The structure analysis conducted in the entire collection with SNP detected two subpopulations. However, the structure analysis conducted with AFLP markers in the subset of 119 accessions proved to have greater degree of resolution and detect six subpopulations. The information provided by both marker types was complementary and showed a strong association between old Argentinian and Italian germplasm and a contribution of CIMMYT germplasm to modern Argentinian, Chilean and Cypriot accessions. The influence of Mediterranean germplasm, mainly from Italy, on part of the modern Argentinian cultivars or breeding lines was also clearly evidenced. Although our analysis yields conclusive results and useful information for association mapping studies, further analyses are needed to refine the number of subpopulations present in the germplasm collection analyzed.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0218562PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6741835PMC
February 2020

Genome Wide Association Study of Karnal Bunt Resistance in a Wheat Germplasm Collection from Afghanistan.

Int J Mol Sci 2019 Jun 26;20(13). Epub 2019 Jun 26.

International Maize and Wheat Improvement Center (CIMMYT), Carretera México-Veracruz Km. 45, El Batán, Texcoco, CP 56237, Mexico.

Karnal bunt disease of wheat, caused by the fungus , is one of the most important challenges to the grain industry as it affects the grain quality and also restricts the international movement of infected grain. It is a seed-, soil- and airborne disease with limited effect of chemical control. Currently, this disease is contained through the deployment of host resistance but further improvement is limited as only a few genotypes have been found to carry partial resistance. To identify genomic regions responsible for resistance in a set of 339 wheat accessions, genome-wide association study (GWAS) was undertaken using the DArTSeq technology, in which 18 genomic regions for Karnal bunt resistance were identified, explaining 5-20% of the phenotypic variation. The identified quantitative trait loci (QTL) on chromosome 2BL showed consistently significant effects across all four experiments, whereas another QTL on 5BL was significant in three experiments. Additional QTLs were mapped on chromosomes 1DL, 2DL, 4AL, 5AS, 6BL, 6BS, 7BS and 7DL that have not been mapped previously, and on chromosomes 4B, 5AL, 5BL and 6BS, which have been reported in previous studies. Germplasm with less than 1% Karnal bunt infection have been identified and can be used for resistance breeding. The SNP markers linked to the genomic regions conferring resistance to Karnal bunt could be used to improve Karnal bunt resistance through marker-assisted selection.
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http://dx.doi.org/10.3390/ijms20133124DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6651844PMC
June 2019

Genetics for low correlation between Fusarium head blight disease and deoxynivalenol (DON) content in a bread wheat mapping population.

Theor Appl Genet 2019 Aug 25;132(8):2401-2411. Epub 2019 May 25.

International Maize and Wheat Improvement Center (CIMMYT), Apdo. Postal 6-641, 06600, Mexico, DF, Mexico.

Key Message: Two QTL with major effects on DON content reduction were identified on chromosomes 3BL and 3DL, with the former showing minor and the latter showing no effects on FHB resistance. Deoxynivalenol (DON) contamination in food and feed is a major concern regarding Fusarium head blight (FHB) infection in wheat. However, relatively less attention has been paid on DON compared to FHB. In this study, a FHB-susceptible cultivar 'NASMA' was hybridized with a FHB-resistant CIMMYT breeding line 'IAS20*5/H567.71' to generate 197 recombinant inbred lines. The population was phenotyped for FHB and associated traits including DON accumulation in spray-inoculated field experiments at CIMMYT-Mexico across four years. Genotyping was performed by using the Illumina Infinium 15 K Beadchip and SSR markers. QTL mapping results indicated that the field FHB resistance was mainly controlled by QTL at Rht-D1 and Vrn-A1, along with a few minor QTL. For DON content, two major QTL were identified: the first located on chromosome 3BL (R of 16-24%), showing minor effects on FHB, and the second was on chromosome 3DL (R of 10-15%), exhibiting no effect on FHB resistance. It is likely that both DON QTL are new based on comparison with previous studies. This study indicates that resistance to DON accumulation and FHB disease could involve different genes, and the utilization of the two DON QTL in breeding could be helpful in further reducing DON contamination in food and feed.
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http://dx.doi.org/10.1007/s00122-019-03362-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6647199PMC
August 2019

Hybrid Wheat Prediction Using Genomic, Pedigree, and Environmental Covariables Interaction Models.

Plant Genome 2019 03;12(1)

In this study, we used genotype × environment interactions (G×E) models for hybrid prediction, where similarity between lines was assessed by pedigree and molecular markers, and similarity between environments was accounted for by environmental covariables. We use five genomic and pedigree models (M1-M5) under four cross-validation (CV) schemes: prediction of hybrids when the training set (i) includes hybrids of all males and females evaluated only in some environments (T2FM), (ii) excludes all progenies from a randomly selected male (T1M), (iii) includes all progenies from 20% randomly selected females in combination with all males (T1F), and (iv) includes one randomly selected male plus 40% randomly selected females that were crossed with it (T0FM). Models were tested on a total of 1888 wheat ( L.) hybrids including 18 males and 667 females in three consecutive years. For grain yield, the most complex model (M5) under T2FM had slightly higher prediction accuracy than the less complex model. For T1F, the prediction accuracy of hybrids for grain yield and other traits of the most complete model was 0.50 to 0.55. For T1M, Model M3 exhibited high prediction accuracies for flowering traits (0.71), whereas the more complex model (M5) demonstrated high accuracy for grain yield (0.5). For T0FM, the prediction accuracy for grain yield of Model M5 was 0.61. Including genomic and pedigree gave relatively high prediction accuracy even when both parents were untested. Results show that it is possible to predict unobserved hybrids when modeling genomic general combining ability (GCA) and specific combining ability (SCA) and their interactions with environments.
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http://dx.doi.org/10.3835/plantgenome2018.07.0051DOI Listing
March 2019

Hyperspectral Reflectance-Derived Relationship Matrices for Genomic Prediction of Grain Yield in Wheat.

G3 (Bethesda) 2019 04 9;9(4):1231-1247. Epub 2019 Apr 9.

Global Wheat Program, International Maize and Wheat Improvement Center (CIMMYT), Ciudad de México, 06600, México

Hyperspectral reflectance phenotyping and genomic selection are two emerging technologies that have the potential to increase plant breeding efficiency by improving prediction accuracy for grain yield. Hyperspectral cameras quantify canopy reflectance across a wide range of wavelengths that are associated with numerous biophysical and biochemical processes in plants. Genomic selection models utilize genome-wide marker or pedigree information to predict the genetic values of breeding lines. In this study, we propose a multi-kernel GBLUP approach to genomic selection that uses genomic marker-, pedigree-, and hyperspectral reflectance-derived relationship matrices to model the genetic main effects and genotype × environment ( × ) interactions across environments within a bread wheat ( L.) breeding program. We utilized an airplane equipped with a hyperspectral camera to phenotype five differentially managed treatments of the yield trials conducted by the Bread Wheat Improvement Program of the International Maize and Wheat Improvement Center (CIMMYT) at Ciudad Obregón, México over four breeding cycles. We observed that single-kernel models using hyperspectral reflectance-derived relationship matrices performed similarly or superior to marker- and pedigree-based genomic selection models when predicting within and across environments. Multi-kernel models combining marker/pedigree information with hyperspectral reflectance phentoypes had the highest prediction accuracies; however, improvements in accuracy over marker- and pedigree-based models were marginal when correcting for days to heading. Our results demonstrate the potential of using hyperspectral imaging to predict grain yield within a multi-environment context and also support further studies on the integration of hyperspectral reflectance phenotyping into breeding programs.
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http://dx.doi.org/10.1534/g3.118.200856DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6469421PMC
April 2019

Resistance to Spot Blotch in Two Mapping Populations of Common Wheat Is Controlled by Multiple QTL of Minor Effects.

Int J Mol Sci 2018 Dec 14;19(12). Epub 2018 Dec 14.

International Maize and Wheat Improvement Center (CIMMYT), Apdo. Postal 6-641, Mexico DF 06600, Mexico.

Spot blotch (SB) is an important fungal disease of wheat in South Asia and South America. Host resistance is regarded as an economical and environmentally friendly approach of controlling SB, and the inheritance of resistance is mostly quantitative. In order to gain a better understanding on the SB resistance mechanism in CIMMYT germplasm, two bi-parental mapping populations were generated, both comprising 232 F progenies. Elite CIMMYT breeding lines, BARTAI and WUYA, were used as resistant parents, whereas CIANO T79 was used as susceptible parent in both populations. The two populations were evaluated for field SB resistance at CIMMYT's Agua Fria station for three consecutive years, from the 2012⁻2013 to 2014⁻2015 cropping seasons. Phenological traits like plant height (PH) and days to heading (DH) were also determined. Genotyping was performed using the DArTSeq genotyping-by-sequencing (GBS) platform, and a few D-genome specific SNPs and those for phenological traits were integrated for analysis. The most prominent quantitative trait locus (QTL) in both populations was found on chromosome 5AL at the locus, explaining phenotypic variations of 7⁻27%. Minor QTL were found on chromosomes 1B, 3A, 3B, 4B, 4D, 5B and 6D in BARTAI and on chromosomes 1B, 2A, 2D and 4B in WUYA, whereas minor QTL contributed by CIANO T79 were identified on chromosome 1B, 1D, 3A, 4B and 7A. In summary, resistance to SB in the two mapping populations was controlled by multiple minor QTL, with strong influence from .
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http://dx.doi.org/10.3390/ijms19124054DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6321084PMC
December 2018

Identification and Validation of a Common Stem Rust Resistance Locus in Two Bi-parental Populations.

Front Plant Sci 2018 30;9:1788. Epub 2018 Nov 30.

International Maize and Wheat Improvement Center (CIMMYT), Mexico City, Mexico.

Races belonging to Ug99 lineage of stem rust fungus f. sp. () continue to pose a threat to wheat ( L.) production in various African countries. Growing resistant varieties is the most economical and environmentally friendly control measure. Recombinant inbred line (RIL) populations from the crosses of susceptible parent 'Cacuke' with the resistant parents 'Huhwa' and 'Yaye' were phenotyped for resistance at the seedling stage to race TTKSK (Ug99) and in adult plants in field trials at Njoro, Kenya for two seasons in 2016. Using the Affymetrix Axiom breeders SNP array, two stem rust resistance genes, temporarily designated as and , were identified and mapped on chromosome arm 2BL through selective genotyping and bulked segregant analysis (BSA), respectively. Kompetitive allele specific polymorphism (KASP) markers and simple sequence repeat (SSR) markers were used to saturate chromosome arm 2BL in both RIL populations. mapped between markers and at a distance of 0.9 cM proximal, and at 2.9 cM distal. was flanked by markers and at 0.8 cM proximal, and at 1.9 cM distal. Two Ug99-effective stem rust resistance genes derived from bread wheat, and , have been reported on chromosome arm 2BL. Infection types and map position in Huhwa and Yaye indicated that was absent in both the parents. However, susceptible reactions produced by resistant lines from both populations against -virulent race TTKSF+ confirmed the presence of a common resistance locus in both lines. Test of allelism is required to establish genetic relationships between genes identified in present study and . Marker linked to was genotyped on set of wheat lines with Huhwa in the pedigree and is advised to be used for marker assisted selection for this gene, however, a combination of phenotypic and genotypic assays is desirable for both genes especially for selection of in breeding programs.
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http://dx.doi.org/10.3389/fpls.2018.01788DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6283910PMC
November 2018