Molecular markers applied to genetic diversity analysis and genome - wide association studies for micronutrients in grains and biotic stresses traits in barley (Hordeum vulgare L.)
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Abstract
The cultivated barley (Hordeum vulgare L.) ranks the fourth most important cereal worldwide. It feeds animals, produces malt, and is used in the human diet. Yield increase and yield stability are the top barley breeding goal. However, diseases such as the Net form of Net blotch (NFNB) and powdery mildew (PM) reduce yield and grain quality. For barley destined for human consumption, micronutrients increase in grains, especially zinc and iron, is essential to alleviate malnutrition. Thus, breeders must select new loci and use them to develop higher-yielding, nutritious, and disease-resistant cultivars. This study reviews the importance of genetic diversity analysis using molecular markers and Genome-wide association studies (GWAS) in barley breeding. Genetic diversity studies are crucial for conservation and utilization of barley germaplasm in plant breeding. Secondly, we discuss genome-wide association study (GWAS) uses to locate genomics regions associated with important barley traits such as disease resistance to NFNB and PM, and micronutrients (Zn and Fe) content in grains. Significant SNP identified in GWAS studies once validated in other experiments or populations, they can be converted into user-friendly markers and used to develop barley cultivars with improved quality, and disease resistance via marker-assisted selection.
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Baik, B.-K.; Ullrich, S.E. Barley for food: Characteristics, improvement, and renewed interest. Journal of cereal science 2008, 48, 233-242.
Dawson, I.K.; Russell, J.; Powell, W.; Steffenson, B.; Thomas, W.T.; Waugh, R. Barley: a translational model for adaptation to climate change. New Phytol. 2015, 206, 913-931.
McCouch, S.; Baute, G.J.; Bradeen, J.; Bramel, P.; Bretting, P.K.; Buckler, E.; Burke, J.M.; Charest, D.; Cloutier, S.; Cole, G. Feeding the future. Nature 2013, 499, 23-24.
Alqudah, A.M.; Sallam, A.; Baenziger, P.S.; Börner, A. GWAS: Fast-forwarding gene identification and characterization in temperate Cereals: lessons from Barley–A review. Journal of advanced research 2020, 22, 119-135.
Smith, K.P.; Thomas, W.; Gutierrez, L.; Bull, H. Genomics-based barley breeding. In The Barley Genome; Springer: 2018; pp. 287-315.
McKevith, B. Nutritional aspects of cereals. Nutrition Bulletin 2004, 29, 111-142.
McKim, S.M.; Koppolu, R.; Schnurbusch, T. Barley inflorescence architecture. In The barley genome; Springer: 2018; pp. 171-208.
Langridge, P. Economic and academic importance of barley. In The barley genome; Springer: 2018; pp. 1-10.
Ullrich, S.E. Barley: Production, improvement, and uses; John Wiley & Sons: 2010; Volume 12.
Haas, M.; Schreiber, M.; Mascher, M. Domestication and crop evolution of wheat and barley: Genes, genomics, and future directions. Journal of integrative plant biology 2019, 61, 204-225.
Kusch, S.; Panstruga, R. mlo-based resistance: an apparently universal “weapon” to defeat powdery mildew disease. Mol. Plant-Microbe Interact. 2017, 30, 179-189.
Lundqvist, U. Scandinavian mutation research in barley–a historical review. Hereditas 2014, 151, 123-131.
Lal, S.; Gulyani, V.; Khurana, P. Overexpression of HVA1 gene from barley generates tolerance to salinity and water stress in transgenic mulberry (Morus indica). Transgenic Res. 2008, 17, 651-663.
Gürel, F.; Öztürk, Z.N.; Uçarlı, C.; Rosellini, D. Barley genes as tools to confer abiotic stress tolerance in crops. Frontiers in plant science 2016, 7, 1137.
IBGSC, I.B.G.S.C. A physical, genetic and functional sequence assembly of the barley genome. Nature 2012, 491, 711-716.
Mascher, M.; Gundlach, H.; Himmelbach, A.; Beier, S.; Twardziok, S.O.; Wicker, T.; Radchuk, V.; Dockter, C.; Hedley, P.E.; Russell, J. A chromosome conformation capture ordered sequence of the barley genome. Nature 2017, 544, 427-433.
Jayakodi, M.; Padmarasu, S.; Haberer, G.; Bonthala, V.S.; Gundlach, H.; Monat, C.; Lux, T.; Kamal, N.; Lang, D.; Himmelbach, A. The barley pan-genome reveals the hidden legacy of mutation breeding. Nature 2020, 588, 284-289.
Sato, K.; Flavell, A.; Russell, J.; Börner, A.; Valkoun, J. Genetic diversity and germplasm management: wild barley, landraces, breeding materials. In Biotechnological approaches to barley improvement; Springer: 2014; pp. 21-36.
Von Bothmer, R.; van Hintum, T.; Knüpffer, H.; Sato, K. Diversity in barley (Hordeum vulgare); Elsevier: 2003.
Endresen, D.T.F.; Street, K.; Mackay, M.; Bari, A.; De Pauw, E. Predictive association between biotic stress traits and eco‐geographic data for wheat and barley landraces. Crop Sci. 2011, 51, 2036-2055.
Blattner, F.R. Taxonomy of the genus Hordeum and barley (Hordeum vulgare). In The Barley Genome; Springer: 2018; pp. 11-23.
Salvi, S.; Druka, A.; Milner, S.G.; Gruszka, D. Induced genetic variation, TILLING and NGS-based cloning. In Biotechnological Approaches to Barley Improvement; Springer: 2014; pp. 287-310.
Langridge, P.; Chalmers, K. The principle: identification and application of molecular markers. In Molecular marker systems in plant breeding and crop improvement; Springer Berlin Heidelberg: 2004; pp. 3-22.
Kretschmer, J.; Chalmers, K.; Manning, S.; Karakousis, A.; Barr, A.; Islam, A.; Logue, S.; Choe, Y.; Barker, S.; Lance, R. RFLP mapping of the Ha 2 cereal cyst nematode resistance gene in barley. Theor. Appl. Genet. 1997, 94, 1060-1064.
Barua, U.; Chalmers, K.; Hackett, C.; Thomas, W.; Powell, W.; Waugh, R. Identification of RAPD markers linked to a Rhynchosporium secalis resistance locus in barley using near-isogenic lines and bulked segregant analysis. Heredity 1993, 71, 177-184.
Henry, R.J. Evolution of DNA marker technology in plants. Molecular markers in plants 2012, 1-19.
Nyiraguhirwa, S.; Grana, Z.; Henkrar, F.; Ouabbou, H.; Mohammed, I.; Udupa, S.M. Genetic diversity and structure of a barley collection predominatly from North African region. Cereal Research Communications 2021, doi:10.1007/s42976-021-00209-2.
Scheben, A.; Batley, J.; Edwards, D. Revolution in genotyping platforms for crop improvement. Plant Genetics and Molecular Biology 2018, 37-52.
Close, T.J.; Bhat, P.R.; Lonardi, S.; Wu, Y.; Rostoks, N.; Ramsay, L.; Druka, A.; Stein, N.; Svensson, J.T.; Wanamaker, S. Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 2009, 10, 1-13.
Comadran, J.; Kilian, B.; Russell, J.; Ramsay, L.; Stein, N.; Ganal, M.; Shaw, P.; Bayer, M.; Thomas, W.; Marshall, D. Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat. Genet. 2012, 44, 1388-1392.
Bayer, M.M.; Rapazote-Flores, P.; Ganal, M.; Hedley, P.E.; Macaulay, M.; Plieske, J.; Ramsay, L.; Russell, J.; Shaw, P.D.; Thomas, W. Development and evaluation of a barley 50k iSelect SNP array. Frontiers in plant science 2017, 8, 1792.
Ganal, M.W.; Plieske, J.; Hohmeyer, A.; Polley, A.; Röder, M.S. High-throughput genotyping for cereal research and breeding. In Applications of genetic and genomic research in cereals; Elsevier: 2019; pp. 3-17.
Waugh, R.; Thomas, B.; Flavell, A.; Ramsay, L.; Comadran, J.; Russell, J. Genome-wide association scans (GWAS). In Biotechnological approaches to Barley improvement; Springer: 2014; pp. 345-365.
Kumar, S.; Volz, R.K.; Chagné, D.; Gardiner, S. Breeding for apple (Malus× domestica Borkh.) fruit quality traits in the genomics era. In Genomics of plant genetic resources; Springer: 2014; pp. 387-416.
Jaganathan, D.; Bohra, A.; Thudi, M.; Varshney, R.K. Fine mapping and gene cloning in the post-NGS era: advances and prospects. Theor. Appl. Genet. 2020, 133, 1791-1810.
Poland, J.A.; Brown, P.J.; Sorrells, M.E.; Jannink, J.-L. Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PloS one 2012, 7, e32253.
Singh, B.; Mehta, S.; Aggarwal, S.K.; Tiwari, M.; Bhuyan, S.I.; Bhatia, S.; Islam, M.A. Barley, disease resistance, and molecular breeding approaches. In Disease resistance in crop plants; Springer: 2019; pp. 261-299.
Riaz, A.; Kanwal, F.; Börner, A.; Pillen, K.; Dai, F.; Alqudah, A.M. Advances in genomics-based breeding of barley: molecular tools and genomic databases. Agronomy 2021, 11, 894.
Kantartzi, S.K. Microsatellites: methods and protocols; Humana Press: 2013.
Tewodros, M.; Zelalem, B. Advances in quantitative trait loci, mapping and importance of markers assisted selection in plant breeding research. International Journal of Plant Breeding and Genetics 2016, 10, 58-68.
Muñoz-Amatriaín, M.; Mascher, M. Sequence diversity and structural variation. In The Barley Genome; Springer: 2018; pp. 109-122.
Kulwal, P.L. Trait mapping approaches through linkage mapping in plants. Plant genetics and molecular biology 2018, 53-82.
Saba Rahim, M.; Sharma, H.; Parveen, A.; Roy, J.K. Trait mapping approaches through association analysis in plants. Plant genetics and molecular biology 2018, 83-108.
Wang, H.; Smith, K.P.; Combs, E.; Blake, T.; Horsley, R.D.; Muehlbauer, G.J. Effect of population size and unbalanced data sets on QTL detection using genome-wide association mapping in barley breeding germplasm. Theor. Appl. Genet. 2012, 124, 111-124.
Pritchard, J.K.; Stephens, M.; Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 2000, 155, 945-959.
Raj, A.; Stephens, M.; Pritchard, J.K. fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 2014, 197, 573-589.
Price, A.L.; Patterson, N.J.; Plenge, R.M.; Weinblatt, M.E.; Shadick, N.A.; Reich, D. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 2006, 38, 904-909.
Chang, C.C.; Chow, C.C.; Tellier, L.C.; Vattikuti, S.; Purcell, S.M.; Lee, J.J. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 2015, 4, s13742-13015-10047-13748.
Wang, D.; Sun, Y.; Stang, P.; Berlin, J.A.; Wilcox, M.A.; Li, Q. Comparison of methods for correcting population stratification in a genome-wide association study of rheumatoid arthritis: principal-component analysis versus multidimensional scaling. In Proceedings of the BMC proceedings, 2009; pp. 1-6.
Yu, J.; Pressoir, G.; Briggs, W.H.; Bi, I.V.; Yamasaki, M.; Doebley, J.F.; McMullen, M.D.; Gaut, B.S.; Nielsen, D.M.; Holland, J.B. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 2006, 38, 203-208.
Del Carpio, D.P.; Lozano, R.; Wolfe, M.D.; Jannink, J.-L. Genome-wide association studies and heritability estimation in the functional genomics era. In Population Genomics; Springer: 2018; pp. 361-425.
Navara, S.; Smith, K.P. Using near-isogenic barley lines to validate deoxynivalenol (DON) QTL previously identified through association analysis. Theor. Appl. Genet. 2014, 127, 633-645.
Xu, Y.; Jia, Q.; Zhou, G.; Zhang, X.-Q.; Angessa, T.; Broughton, S.; Yan, G.; Zhang, W.; Li, C. Characterization of the sdw1 semi-dwarf gene in barley. BMC Plant Biol. 2017, 17, 1-10.
Rossini, L.; Muehlbauer, G.J.; Okagaki, R.; Salvi, S.; von Korff, M. Genetics of whole plant morphology and architecture. In The Barley Genome; Springer: 2018; pp. 209-231.
Grewal, T.; Rossnagel, B.; Pozniak, C.; Scoles, G. Mapping quantitative trait loci associated with barley net blotch resistance. Theor. Appl. Genet. 2008, 116, 529-539.
Afanasenko, O. Blumeria graminis f. sp. hordei - Powdery mildew of barley. Available online: http://www.agroatlas.ru/en/content/diseases/Hordei/Hordei_Blumeria_graminis/index.html (accessed on 15,August).
White, P.J.; Broadley, M.R. Biofortification of crops with seven mineral elements often lacking in human diets–iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol. 2009, 182, 49-84.
Khan, P.S.V.; Nagamallaiah, G.; Rao, M.D.; Sergeant, K.; Hausman, J. Abiotic stress tolerance in plants: insights from proteomics. In Emerging technologies and management of crop stress tolerance; Elsevier: 2014; pp. 23-68.
Saade, S.; Maurer, A.; Shahid, M.; Oakey, H.; Schmöckel, S.M.; Negrão, S.; Pillen, K.; Tester, M. Yield-related salinity tolerance traits identified in a nested association mapping (NAM) population of wild barley. Scientific reports 2016, 6, 1-9.
Paulitz, T.C.; Steffenson, B.J. Biotic stress in barley: disease problems and solutions. Barley production, improvement, and uses 2011, 307-354.
Ilyas, M.; Rafique, K.; Ahmed, S.; Zulfiqar, S.; Afzal, F.; Khalid, M.; Kazi, A.G.; Mujeeb-Kazi, A. Preventing potential diseases of crop plants under the impact of a changing environment. Emerging Technologies and Management of Crop Stress Tolerance 2014, 193-214.
Lamichhane, J.R.; Dachbrodt-Saaydeh, S.; Kudsk, P.; Messéan, A. Toward a reduced reliance on conventional pesticides in European agriculture. Plant Dis. 2016, 100, 10-24.
Sánchez-Martín, J.; Keller, B. Contribution of recent technological advances to future resistance breeding. Theor. Appl. Genet. 2019, 132, 713-732.
Ruge-Wehling, B.; Wehling, P. The secondary gene pool of barley (Hordeum bulbosum): Gene introgression and homoeologous recombination. In Biotechnological Approaches to Barley Improvement; Springer: 2014; pp. 331-343.
Kis, A.; Hamar, É.; Tholt, G.; Bán, R.; Havelda, Z. Creating highly efficient resistance against wheat dwarf virus in barley by employing CRISPR/Cas9 system. Plant Biotechnol. J. 2019, 17, 1004.
Zhang, Y.; Lubberstedt, T.; Xu, M. The genetic and molecular basis of plant resistance to pathogens. Journal of Genetics and Genomics 2013, 40, 23-35.
Ordon, F.; Kühne, T. Response to viral pathogens. In Biotechnological Approaches to Barley Improvement; Springer: 2014; pp. 181-196.
Oerke, E.-C. Crop losses to pests. The Journal of Agricultural Science 2006, 144, 31-43.
Liu, Z.; Ellwood, S.R.; Oliver, R.P.; Friesen, T.L. Pyrenophora teres: profile of an increasingly damaging barley pathogen. Mol. Plant Pathol. 2011, 12, 1-19.
Backes, A.; Guerriero, G.; Barka, E.A.; Jacquard, C. Pyrenophora teres: taxonomy, morphology, interaction with barley, and mode of control. Frontiers in Plant Science 2021, 12.
Mathre, D.E.; Mathre, D.E. Compendium of barley diseases; APS press St. Paul, MN: 1997.
Elmore, J.M.; Perovic, D.; Ordon, F.; Schweizer, P.; Wise, R.P. A genomic view of biotic stress resistance. In The barley genome; Springer: 2018; pp. 233-257.
Perovic, D.; Kopahnke, D.; Habekuss, A.; Ordon, F.; Serfling, A. Marker-based harnessing of genetic diversity to improve resistance of barley to fungal and viral diseases. In Applications of Genetic and Genomic Research in Cereals; Elsevier: 2019; pp. 137-164.
Clare, S.J.; Wyatt, N.A.; Brueggeman, R.S.; Friesen, T.L. Research advances in the Pyrenophora teres–barley interaction. Mol. Plant Pathol. 2020, 21, 272-288.
Amezrou, R.; Verma, R.P.S.; Chao, S.; Brueggeman, R.S.; Belqadi, L.; Arbaoui, M.; Rehman, S.; Gyawali, S. Genome-wide association studies of net form of net blotch resistance at seedling and adult plant stages in spring barley collection. Mol. Breed. 2018, 38, 58.
Adhikari, A.; Steffenson, B.J.; Smith, M.J.; Dill-Macky, R. Genome-wide association mapping of seedling net form net blotch resistance in an Ethiopian and Eritrean Barley Collection. Crop Sci. 2019, 59, 1625-1638.
Novakazi, F.; Afanasenko, O.; Anisimova, A.; Platz, G.J.; Snowdon, R.; Kovaleva, O.; Zubkovich, A.; Ordon, F. Genetic analysis of a worldwide barley collection for resistance to net form of net blotch disease (Pyrenophora teres f. teres). Theor. Appl. Genet. 2019, 132, 2633-2650.
Oerke, E.-C. Estimated crop losses due to pathogens, animal pests and weeds. Crop Production and Crop Protection. Elsevier Science Publishing, New York, NY 1994, 535-597.
Sabelleck, B.; Panstruga, R. Novel jack-in-the-box effector of the barley powdery mildew pathogen? J. Exp. Bot. 2018, 69, 3511-3514.
EPPO. Blumeria graminis f. sp. hordei. 2018.
Novakazi, F.; Krusell, L.; Jensen, J.D.; Orabi, J.; Jahoor, A.; Bengtsson, T.; Consortium, P.B. You had me at “MAGIC”!: four barley MAGIC populations reveal novel resistance QTL for powdery mildew. Genes 2020, 11, 1512.
Gupta, S.; Vassos, E.; Sznajder, B.; Fox, R.; Khoo, K.H.; Loughman, R.; Chalmers, K.J.; Mather, D.E. A locus on barley chromosome 5H affects adult plant resistance to powdery mildew. Mol. Breed. 2018, 38, 1-10.
Silvar, C.; Casas, A.; Igartua, E.; Ponce-Molina, L.; Gracia, M.; Schweizer, G.; Herz, M.; Flath, K.; Waugh, R.; Kopahnke, D. Resistance to powdery mildew in Spanish barley landraces is controlled by different sets of quantitative trait loci. Theor. Appl. Genet. 2011, 123, 1019-1028.
Tam, E.; Keats, E.C.; Rind, F.; Das, J.K.; Bhutta, Z.A. Micronutrient supplementation and fortification interventions on health and development outcomes among children under-five in low-and middle-income countries: a systematic review and meta-analysis. Nutrients 2020, 12, 289.
WHO. Malnutrution. Available online: https://www.who.int/news-room/fact-sheets/detail/malnutrition (accessed on 1,april).
Hirschi, K.D. Nutrient biofortification of food crops. Annu. Rev. Nutr. 2009, 29, 401-421.
Andersson, M.S.; Pfeiffer, W.H.; Tohme, J. Enhancing nutritional quality in crops via genomics approaches. In Genomics of plant genetic resources; Springer: 2014; pp. 417-429.
Bouis, H. Reducing mineral and vitamin deficiencies through biofortification: progress under HarvestPlus. In Hidden hunger: strategies to improve nutrition quality; Karger Publishers: 2018; Volume 118, pp. 112-122.
Khan, M.K.; Pandey, A.; Hamurcu, M.; Hakki, E.E.; Gezgin, S. Role of molecular approaches in improving genetic variability of micronutrients and their utilization in breeding programs. In Wheat and Barley Grain Biofortification; Elsevier: 2020; pp. 27-52.
Ye, X.; Al-Babili, S.; Klöti, A.; Zhang, J.; Lucca, P.; Beyer, P.; Potrykus, I. Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 2000, 287, 303-305.
Paine, J.A.; Shipton, C.A.; Chaggar, S.; Howells, R.M.; Kennedy, M.J.; Vernon, G.; Wright, S.Y.; Hinchliffe, E.; Adams, J.L.; Silverstone, A.L. Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat. Biotechnol. 2005, 23, 482-487.
Holme, I.B.; Wendt, T.; Gil-Humanes, J.; Deleuran, L.C.; Starker, C.G.; Voytas, D.F.; Brinch-Pedersen, H. Evaluation of the mature grain phytase candidate HvPAPhy_a gene in barley (Hordeum vulgare L.) using CRISPR/Cas9 and TALENs. Plant Mol. Biol. 2017, 95, 111-121.
Abe, K.; Araki, E.; Suzuki, Y.; Toki, S.; Saika, H. Production of high oleic/low linoleic rice by genome editing. Plant Physiol. Biochem. 2018, 131, 58-62.
Takahashi, M.; Nakanishi, H.; Kawasaki, S.; Nishizawa, N.K.; Mori, S. Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nat. Biotechnol. 2001, 19, 466-469.
Masuda, H.; Usuda, K.; Kobayashi, T.; Ishimaru, Y.; Kakei, Y.; Takahashi, M.; Higuchi, K.; Nakanishi, H.; Mori, S.; Nishizawa, N.K. Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice 2009, 2, 155-166.
Mamo, B.E.; Barber, B.L.; Steffenson, B.J. Genome-wide association mapping of zinc and iron concentration in barley landraces from Ethiopia and Eritrea. Journal of cereal science 2014, 60, 497-506.
Gyawali, S.; Otte, M.L.; Chao, S.; Jilal, A.; Jacob, D.L.; Amezrou, R.; Verma, R.P.S. Genome wide association studies (GWAS) of element contents in grain with a special focus on zinc and iron in a world collection of barley (Hordeum vulgare L.). Journal of cereal science 2017, 77, 266-274.
Wiegmann, M.; Thomas, W.T.; Bull, H.J.; Flavell, A.J.; Zeyner, A.; Peiter, E.; Pillen, K.; Maurer, A. Wild barley serves as a source for biofortification of barley grains. Plant Sci. 2019, 283, 83-94.
Hussain, S.; Rengel, Z.; Mohammadi, S.A.; Ebadi-Segherloo, A.; Maqsood, M.A. Mapping QTL associated with remobilization of zinc from vegetative tissues into grains of barley (Hordeum vulgare). Plant Soil 2016, 399, 193-208.