Identification of SNPs Associated with Grain Quality Traits in Spring Barley Collection Grown in Southeastern Kazakhstan

: Barley ( Hordeum vulgare L.) is an important cereal crop with high genome plasticity that is cultivated in all climatic zones. Traditionally, barley grain is used for animal feed, malting, brewing, and food production. Depending on the end-use product, there are individual requirements for the quality traits of barley grain, particularly for raw starch and protein contents. This study evaluates a collection of 406 two-rowed spring barley accessions, comprising cultivars and lines from the USA, Kazakhstan, Europe, and Africa, based on five grain quality traits (the contents of raw starch, protein, cellulose, and lipids, and grain test weight) over two years. The results of population structure analysis demonstrate the significant impact of geographical origin on the formation of subclusters in the studied population. It was also found that the environment significantly affects grain quality traits. Heat and drought stresses, particularly during grain filling, led to higher protein and lower starch contents. A genome-wide association study (GWAS) using a multiple-locus mixed linear model (MLMM) allowed for the identification of 26 significant quantitative trait loci (QTLs) for the five studied grain quality traits. Among them, 17 QTLs were found to be positioned close to known genes and previously reported QTLs for grain quality in the scientific literature. Most of the identified candidate genes were dehydration stress and flowering genes, confirming that exposure to heat and drought stresses during grain filling may lead to dramatic changes in grain quality traits, including lower starch and higher protein contents. Nine QTLs were presumably novel and could be used for gene mining and breeding activities, including marker-assisted selection to improve grain quality parameters.

[1]  T. Blake,et al.  Identification of SNP Markers Associated with Grain Quality Traits in a Barley Collection (Hordeum vulgare L.) Harvested in Kazakhstan , 2022, Agronomy.

[2]  P. Hayes,et al.  Barley grain protein is influenced by genotype, environment, and nitrogen management and is the major driver of malting quality , 2022, Crop Science.

[3]  T. Vanhala,et al.  Protein content and HvNAM alleles in Nordic barley (Hordeum vulgare) during a century of breeding , 2022, Hereditas.

[4]  Kazuhiro Sato,et al.  Population Structure and Genetic Diversity of Two-Rowed Barley Accessions from Kazakhstan Based on SNP Genotyping Data , 2021, Plants.

[5]  X. Ou,et al.  Genome-wide identification of alcohol dehydrogenase (ADH) gene family under waterlogging stress in wheat (Triticum aestivum) , 2021, PeerJ.

[6]  Aylin W. Sahin,et al.  Barley Protein Properties, Extraction and Applications, with a Focus on Brewers’ Spent Grain Protein , 2021, Foods.

[7]  Yasser S. Moursi,et al.  Genetic associations uncover candidate SNP markers and genes associated with salt tolerance during seedling developmental phase in barley , 2021 .

[8]  Muhammad Faisal Manzoor,et al.  Compositional profile of barley landlines grown in different regions of Gilgit‐Baltistan , 2021, Food science & nutrition.

[9]  G. Fincher,et al.  Genes That Mediate Starch Metabolism in Developing and Germinated Barley Grain , 2021, Frontiers in Plant Science.

[10]  Jianming Yu,et al.  Status and prospects of genome‐wide association studies in plants , 2021, The plant genome.

[11]  Mekonnen Gebeyaw,et al.  Impact of Malt Barley Varieties on Malt Quality: A Review , 2021, Agricultural Reviews.

[12]  Guo-ping Zhang,et al.  Genome-Wide Association Study on Total Starch, Amylose and Amylopectin in Barley Grain Reveals Novel Putative Alleles , 2021, International journal of molecular sciences.

[13]  Zhiwu Zhang,et al.  GAPIT Version 3: Boosting Power and Accuracy for Genomic Association and Prediction , 2020, bioRxiv.

[14]  Joshua V. Peñalba,et al.  From molecules to populations: appreciating and estimating recombination rate variation , 2020, Nature Reviews Genetics.

[15]  A. Jahoor,et al.  Genomic prediction and GWAS of yield, quality and disease-related traits in spring barley and winter wheat , 2020, Scientific Reports.

[16]  Kevin P. Smith,et al.  Identification of quantitative trait loci for net form net blotch resistance in contemporary barley breeding germplasm from the USA using genome-wide association mapping , 2020, Theoretical and Applied Genetics.

[17]  N. Tashi,et al.  A mutation in Waxy gene affects amylose content, starch granules and kernel characteristics of barley ( Hordeum vulgare ) , 2019, Plant Breeding.

[18]  M. Hrmova,et al.  DREB/CBF expression in wheat and barley using the stress‐inducible promoters of HD‐Zip I genes: impact on plant development, stress tolerance and yield , 2019, Plant biotechnology journal.

[19]  S. Chao,et al.  Association mapping for agronomic traits in six-rowed spring barley from the USA harvested in Kazakhstan , 2019, PloS one.

[20]  J. Walling,et al.  Comparative gene expression analysis of the β-amylase and hordein gene families in the developing barley grain. , 2019, Gene.

[21]  F. Alghabari,et al.  Effects of drought stress on growth, grain filling duration, yield and quality attributes of barley (Hordeum vulgare L.) , 2018, Bangladesh Journal of Botany.

[22]  S. Chao,et al.  Marker-trait associations in two-rowed spring barley accessions from Kazakhstan and the USA , 2018, PloS one.

[23]  R. Burton,et al.  Revised Phylogeny of the Cellulose Synthase Gene Superfamily: Insights into Cell Wall Evolution1[OPEN] , 2018, Plant Physiology.

[24]  S. Chao,et al.  Genome wide association studies (GWAS) of spot blotch resistance at the seedling and the adult plant stages in a collection of spring barley , 2018, Molecular Breeding.

[25]  S. Chao,et al.  Genome-wide association studies of net form of net blotch resistance at seedling and adult plant stages in spring barley collection , 2018, Molecular Breeding.

[26]  Paul D. Shaw,et al.  Development and Evaluation of a Barley 50k iSelect SNP Array , 2017, Front. Plant Sci..

[27]  R. Waugh,et al.  A Genome Wide Association Study of arabinoxylan content in 2-row spring barley grain , 2017, PloS one.

[28]  G. Guo,et al.  Identification of QTLs controlling grain protein concentration using a high-density SNP and SSR linkage map in barley (Hordeum vulgare L.) , 2017, BMC Plant Biology.

[29]  Chenwu Xu,et al.  Genetic mapping of quantitative trait loci in crops , 2017 .

[30]  T. Schnurbusch,et al.  VRS2 regulates hormone-mediated inflorescence patterning in barley , 2016, Nature Genetics.

[31]  S. Shabala,et al.  Genome-Wide Association Study Reveals a New QTL for Salinity Tolerance in Barley (Hordeum vulgare L.) , 2016, Front. Plant Sci..

[32]  T. Schnurbusch,et al.  The Genetic Architecture of Barley Plant Stature , 2016, Front. Genet..

[33]  G. Orjeda,et al.  Multi-environment multi-QTL association mapping identifies disease resistance QTL in barley germplasm from Latin America , 2015, Theoretical and Applied Genetics.

[34]  G. Fox,et al.  Drought‐proofing barley (Hordeum vulgare) and its impact on grain quality: A review , 2015 .

[35]  T. Schnurbusch,et al.  Genetic Dissection of Photoperiod Response Based on GWAS of Pre-Anthesis Phase Duration in Spring Barley , 2014, PloS one.

[36]  P. Hayes,et al.  Barley genetic variation: implications for crop improvement. , 2014, Briefings in functional genomics.

[37]  Guo-ping Zhang,et al.  Grain protein content variation and its association analysis in barley , 2013, BMC Plant Biology.

[38]  B. vonHoldt,et al.  STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method , 2012, Conservation Genetics Resources.

[39]  E. Vincze,et al.  Quantitative RT-PCR based platform for rapid quantification of the transcripts of highly homologous multigene families and their members during grain development , 2012, BMC Plant Biology.

[40]  Bjarni J. Vilhjálmsson,et al.  An efficient multi-locus mixed model approach for genome-wide association studies in structured populations , 2012, Nature Genetics.

[41]  F. V. van Eeuwijk,et al.  Genome-wide association studies for agronomical traits in a world wide spring barley collection , 2012, BMC Plant Biology.

[42]  Kevin P. Smith,et al.  Genome-wide association mapping of Fusarium head blight resistance in contemporary barley breeding germplasm , 2011, Molecular Breeding.

[43]  L. Ramsay,et al.  NAM-1gene polymorphism and grain protein content in Hordeum. , 2010, Journal of plant physiology.

[44]  J. Rafalski,et al.  Association genetics in crop improvement. , 2010, Current opinion in plant biology.

[45]  H. Abdel-Haleem,et al.  Quantitative trait loci of acid detergent fiber and grain chemical composition in hulled × hull-less barley population , 2010, Euphytica.

[46]  Timothy J. Close,et al.  Population Structure and Linkage Disequilibrium in U.S. Barley Germplasm: Implications for Association Mapping , 2010 .

[47]  T. Close,et al.  An Integrated Resource for Barley Linkage Map and Malting Quality QTL Alignment , 2009 .

[48]  G. Slafer,et al.  Yield and biomass in wheat and barley under a range of conditions in a Mediterranean site , 2009 .

[49]  N. Tinker,et al.  Population structure and linkage disequilibrium in barley assessed by DArT markers , 2009, Theoretical and Applied Genetics.

[50]  Jean-Luc Jannink,et al.  The emergence of whole genome association scans in barley. , 2009, Current opinion in plant biology.

[51]  M. Giroux,et al.  Associations Between Vrs1 Alleles and Grain Quality Traits in Spring Barley Hordeum vulgare L , 2008 .

[52]  Felipe Rodrigues da Silva,et al.  Identification of drought-responsive genes in roots of upland rice (Oryza sativa L) , 2008, BMC Genomics.

[53]  A. Wahid,et al.  Dehydrin gene expression provides an indicator of low temperature and drought stress: transcriptome-based analysis of Barley (Hordeum vulgare L.) , 2008, Functional & Integrative Genomics.

[54]  H. Kanamori,et al.  Barley grain with adhering hulls is controlled by an ERF family transcription factor gene regulating a lipid biosynthesis pathway , 2008, Proceedings of the National Academy of Sciences.

[55]  Antony Bacic,et al.  The Genetics and Transcriptional Profiles of the Cellulose Synthase-Like HvCslF Gene Family in Barley1[OA] , 2008, Plant Physiology.

[56]  Edward S. Buckler,et al.  TASSEL: software for association mapping of complex traits in diverse samples , 2007, Bioinform..

[57]  Teresa Penfield,et al.  The Transcription Factor WIN1/SHN1 Regulates Cutin Biosynthesis in Arabidopsis thaliana[W] , 2007, The Plant Cell Online.

[58]  Andreas Graner,et al.  Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene , 2007, Proceedings of the National Academy of Sciences.

[59]  J. Dubcovsky,et al.  A NAC Gene Regulating Senescence Improves Grain Protein, Zinc, and Iron Content in Wheat , 2006, Science.

[60]  M. Ganal,et al.  Analysis of QTLs for yield components, agronomic traits, and disease resistance in an advanced backcross population of spring barley. , 2006, Genome.

[61]  M. Ganal,et al.  Analysis of molecular diversity, population structure and linkage disequilibrium in a worldwide survey of cultivated barley germplasm (Hordeum vulgare L.) , 2006, BMC Genetics.

[62]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[63]  Rod A Wing,et al.  A New Resource for Cereal Genomics: 22K Barley GeneChip Comes of Age1 , 2004, Plant Physiology.

[64]  D. Moody,et al.  Identification of QTLs associated with variations in grain protein concentration in two-row barley , 2003 .

[65]  G. McVean,et al.  Estimating recombination rates from population-genetic data , 2003, Nature Reviews Genetics.

[66]  M. Stephens,et al.  Traces of Human Migrations in Helicobacter pylori Populations , 2003, Science.

[67]  S. Ullrich,et al.  QTL analysis of agronomic traits in barley based on the doubled haploid progeny of two elite North American varieties representing different germplasm groups , 2001, Theoretical and Applied Genetics.

[68]  Alison M. Smith,et al.  The biosynthesis of starch granules. , 2001, Biomacromolecules.

[69]  Z. Kaczmarek,et al.  Genotype-environment interaction of barley doubled haploids with regard to malting quality , 1999 .

[70]  D. Mather,et al.  Mapping quantitative trait loci for starch granule traits in Barley , 1999 .

[71]  R. Savin,et al.  Effects of Short Periods of Drought and High Temperature on Grain Growth and Starch Accumulation of Two Malting Barley Cultivars , 1996 .

[72]  J. Jacobsen,et al.  Effects of Heat and Water Stress on Malt Quality and Grain Parameters of Schooner Barley Grown in Cabinets , 1993 .

[73]  R. Henry The Carbohydrates of barley grains - A review , 1988 .

[74]  P. Langridge Economic and Academic Importance of Barley , 2018 .

[75]  F. Haddadin Assessment of Drought Tolerant Barley Varieties under Water Stress , 2015 .

[76]  J. Doe Association Mapping of Agronomic QTLs in U.S. Spring Barley Breeding Germplasm , 2014 .

[77]  S. Chao,et al.  Marker-trait associations in Virginia Tech winter barley identified using genome-wide mapping , 2012, Theoretical and Applied Genetics.

[78]  Z. Gaile,et al.  Grain quality traits important in feed barley , 2012 .

[79]  Kevin P. Smith,et al.  Effect of population size and unbalanced data sets on QTL detection using genome-wide association mapping in barley breeding germplasm , 2011, Theoretical and Applied Genetics.

[80]  H. Handa,et al.  Molecular and Functional Characterization of PEBP Genes in Barley Reveal the Diversification of Their Roles in Flowering , 2009 .

[81]  Meixue Zhou,et al.  Protein and hordein content in barley seeds as affected by nitrogen level and their relationship to beta-amylase activity , 2006 .

[82]  M. Flores-Vergara,et al.  A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide , 2006, Nature Protocols.

[83]  N. Samarah Effects of drought stress on growth and yield of barley , 2005 .

[84]  F. Hana,et al.  Quantitative genetic analysis of acid detergent fibre content in barley grain , 2003 .

[85]  S. Ullrich,et al.  QTL analysis of malting quality in barley based on the doubled-haploid progeny of two elite North American varieties representing different germplasm groups , 2000, Theoretical and Applied Genetics.

[86]  Jordi Voltas,et al.  Genetic and environmental variation in malting and feed quality of barley , 1997 .

[87]  P. N. Fox,et al.  Genotype × environment interaction and adaptation , 1993 .

[88]  G. Fedak LIPID AND FATTY ACID COMPOSITION OF BARLEY KERNELS , 1977 .