Genome Wide Association Study in Pulses for Salt Tolerance: Status and Perspective


Abstract views: 268 / PDF downloads: 129

Authors

  • Pooja Kanwar Shekhawat ICAR-Central Soil salinity Research Institute, Karnal, Haryana, India-132001
  • Jogendra Singh Division of Crop Improvement, ICAR-Central Soil salinity Research Institute, Karnal, Haryana, India-132001
  • Mohan Lal Jakhar Department of Plant Breeding and Genetics, Sri Karan Narendra Agriculture University, Jobner, Jaipur, Rajasthan-303329, India
  • Sumer Singh Punia Department of Plant Breeding and Genetics, Sri Karan Narendra Agriculture University, Jobner, Jaipur, Rajasthan-303329, India
  • Vijayata Singh Division of Crop Improvement, ICAR-Central Soil salinity Research Institute, Karnal, Haryana, India-132001

Abstract

Genome wide association study (GWAS) is a powerful, reliable, leading and effective approach for unraveling the genetic makeup of complicated phenotypic features back to their underlying genetics. Morphological, physiological, biochemical and quality traits of pulses are severely affected by biotic and abiotic stresses significantly affecting their growth, yield and productivity. Soli salinity is most challenging factor among all abiotic stresses that significantly reduces the yield of pulses. These are a promising source for human diet due to their richness in the content of protein, micronutrients (Fe, Zn etc.), carbohydrates, fibres and antioxidants in addition to their long shelf life, suitability to marginal environments etc. It is crucial to comprehend the genetic foundation of underlying features to boost the production of pulses for world food and nutritional security. Implementing GWAS in pulses can lead to the effective discovery of countless genomic areas linked to salinity stress. It have been applied in pulses to dissect the traits related to yield, such as seed size and pod number, traits associated with resistance to biotic and abiotic stresses, like disease resistance, drought and salt tolerance as well as for micronutrients like Fe, Zn etc. This review presents the overview of the application of GWAS for the pulse’s improvement programme, its strengths, weakness and applications that can facilitate the dissection of the gene networks underlying complex traits like salinity and alkalinity and improve its efficiency in a molecular breeding programme.

Downloads

Download data is not yet available.

References

Abou-Khater L, Maalouf F, Jighly A, Alsamman AM, Rubiales D, Rispail N, Hu J, Ma Y, Balech R, Hamwieh A, Baum M and Kumar S (2022) Genomic regions associated with herbicide tolerance in a worldwide faba bean (Vicia faba L.) collection. Scientific Reports 12(1):158.

Adobor S, Gela, TS, Banniza, S and Vandenberg, A (2023) Mapping of genomic regions linked to stemphylium blight (Stemphylium botryosum Wallr.) resistance in lentil using linkage mapping and marker-trait association analysis. Euphytica 219(8): 86.

Ahmed SM, Alsamman AM, Jighly A, Mubarak MH, Al-Shamaa K, Istanbuli T, Momtaz O A, El Allali A and Hamwieh A (2021) Genome-wide association analysis of chickpea germplasms differing for salinity tolerance based on DArTseq markers. Plos one 16(12): e0260709.

Alqudah, A., Sallam A, Baenziger PS and Borner, A (2020) GWAS: Fast-forwarding gene identification and characterization in temperate Cereals: lessons from Barley–A review. Journal of Advanced Research 22: 119–135.

Anderson K (2010) Globalization's effects on world agricultural trade, 1960- 2050. Philosophical Transactions of the Royal Society B: Biological Sciences, 365 (1554): 3007-3021.

Arkwazee HA, Wallace LT, Hart JP, Griffiths PD and Myers JR (2022) Genome-Wide Association Study (GWAS) of White Mold Resistance in Snap Bean. Genes 13 (12): 2297.

Ates D, Asciogul TK, Nemli S, Erdogmus S, Esiyok D and Tanyolac MB (2018) Association mapping of days to flowering in common bean (Phaseolus vulgaris L.) revealed by DArT markers. Molecular Breeding 38: 113.

Basu U, Bajaj D, Sharma A, Malik N, Daware A, Narnoliya L, Thakro V, Upadhyaya HD, Kumar R, Tripathi S, Bharadwaj C, Tyagi AK and Parida SK (2019) Genetic dissection of photosynthetic efficiency traits for enhancing seed yield in chickpea. Plant Cell Environment 42(1):158-173.

Bennett AJ, Bending GD, Chandler D, Hilton S and Mills P (2012) Meeting the demand for crop production: the challenge of yield decline in crops grown in short rotations. Biological reviews 87(1): 52-71.

Berendzen J, Brown AV, Cameron CT, Campbell JD, Cleary AM, Dash S, Hokin S, Huang W, Kalberer SR, Nelson RT and Redsun S (2021) The legume information system and associated online genomic resources. Legume Science 3(3): e74.

Bhat JA, Yu D, Bohra A, Ganie SA and Varshney RK (2021) Features and applications of haplotypes in crop breeding. Communications biology 4(1): 1266.

Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M, Bergelson J, Cuguen J and Roux F (2010) Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genetics 6(5): e1000940.

Brachi B, Morris GP and Borevitz JO (2011) Genome-wide association studies in plants: The missing heritability is in the field. Genome Biology 12: 232.

Breria CM, Hsieh CH, Yen TB, Yen JY, Noble TJ and Schafleitner R (2020) A SNP-based genome-wide association study to mine genetic loci associated to salinity tolerance in mungbean (Vigna radiata L.). Genes 11(7): 759.

Campa A, Garcia-Fernandez C and Ferreira JJ (2020) Genome-wide association study (GWAS) for resistance to Sclerotinia sclerotiorum in common bean. Genes 11(12): 1496.

Cardon LR, Palmer LJ (2003) Population stratification and spurious allelic association. The Lancet 361(9357): 598-604.

Chang Y, Peng L, Ji L, Wang S, Wang L and Wu J (2023) Genome-wise association study identified genomic regions associated with drought tolerance in mungbean (Vigna radiata (L.) R. Wilczek). Theoretical and Applied Genetics 136(3): 40.

Channale S, Thompson JP, Varshney RK, Thudi M and Zwart RS (2023) Multi-locus genome-wide association study of chickpea reference set identifies genetic determinants of Pratylenchus thornei resistance. Frontiers in Plant Science 14: 1139574.

Chen Y, Xiong H, Ravelombola W, Bhattarai G, Barickman C, Alatawi I, Phiri TM, Chiwina K, Mou B, Tallury S and Shi A (2023) A Genome-Wide Association Study Reveals Region Associated with Seed Protein Content in Cowpea. Plants (Basel) 12(14): 2705.

Cichy KA, Wiesinger JA and Mendoza FA (2015) Genetic diversity and genome-wide association analysis of cooking time in dry bean (Phaseolus vulgaris L.). Theoretical in Applied Genetics 128: 1555-1567.

Cobos M, Satovic Z, Rubiales D and Fondevilla S (2018) Er3 gene, conferring resistance to powdery mildew in pea, is located in pea LGIV. Euphytica 214: 203.

De Almeida CP, de Carvalho Paulino JF, Bonfante GFJ, Perseguini JMKC, Santos IL, Gonçalves JGR, Patrício FRA, Taniguti CH, Gesteira GS, Garcia AAF, Song Q, Carbonell S AM, Chiorato AF and Benchimol-Reis LL (2021) Angular leaf spot resistance loci associated with different plant growth stages in common bean. Frontiers in Plant Science 12: 647043.

Diapari M, Sindhu A, Bett K, Deokar A, Warkentin TD and Tar’an B (2014) Genetic diversity and association mapping of iron and zinc concentrations in chickpea (Cicer arietinum L.). Genome, 57 (8): 459-468.

Diaz LM, Ricaurte J, Tovar E, Cajiao C, Teran H, Grajales M, Polanía J, Rao I, Beebe S and Raatz B (2018) QTL analyses for tolerance to abiotic stresses in a common bean (Phaseolus vulgaris L.) population. PLoS One 13: e0202342.

Diaz S, Ariza-Suarez D, Izquierdo P, Lobaton JD, de la Hoz JF, Acevedo F, Duitama J, Guerrero AF, Cajiao C, Mayor V and Beebe SE (2020) Genetic mapping for agronomic traits in a MAGIC population of common bean (Phaseolus vulgaris L.) under drought conditions. BMC genomics 21(1):1-20.

Dikshit H, Singh A, Singh D, Aski M, Jain N, Hegde V S, Basandrai A, Basandrai D and Sharma T (2016) Tagging and mapping of SSR marker for rust resistance gene in lentil (Lens culinaris Medikus subsp. culinaris). Indian Journal of Experimental Biology 54: 394-399.

Dissanayake R., Cogan NO, Smith KF and Kaur S (2021) Application of genomics to understand salt tolerance in lentil. Genes 12(3): 332.

Ek M, Eklund M, Von Post R, Dayteg C, Henriksson T, Weibull P, Ceplitis A, Isaac P and Tuvesson S (2005) Microsatellite markers for powdery mildew resistance in pea (Pisum sativum L.). Hereditas 142: 86-91.

Elhaik E (2022) Principal Component Analyses (PCA)-based findings in population genetic studies are highly biased and must be reevaluated. Scientific Reports 12: 14683.

Ender M, Terpstra K and Kelly JD (2008) Marker-assisted selection for white mold resistance in common bean. Molecular Breeding 21: 149-157.

Erdogmus S, Ates D, Nemli S, Yagmur B, Asciogul TK, Ozkuru E, Karaca N, Yilmaz H, Esiyok D Ek M, Eklund M, Von Post R, Dayteg C, Henriksson T, Weibull P, Ceplitis A, Isaac P and Tuvesson S (2005) Microsatellite markers for powdery mildew resistance in pea (Pisum sativum L.). Hereditas 142: 86-91.

Tanyolac MB (2020) Genome-wide association studies of Ca and Mn in the seeds of the common bean (Phaseolus vulgaris L.). Genomics 112(6): 4536-46.

Farahani S, Maleki M, Ford R, Mehrabi R, Kanouni H, Kema GH, Naji AM, and Talebi R (2022) Genome-wide association mapping for isolate-specific resistance to Ascochyta rabiei in chickpea (Cicer arietinum L.). Physiological and Molecular Plant Pathology 121: 101883.

Farooq MS, Uzair M, Raza A, Habib M, Xu Y, Yousuf M, Yang SH and Ramzan Khan M (2022) Uncovering the research gaps to alleviate the negative impacts of climate change on food security: a review. Frontiers in plant science 13: 927535.

Fayaz H, Tyagi S, Wani AA, Pandey R, Akhtar S, Bhat MA, Chitikineni A, Varshney RK, Thudi M, Kumar U and Mir RR (2022) Genome-wide association analysis to delineate high-quality SNPs for seed micronutrient density in chickpea (Cicer arietinum L.). Scientific Reports 12: 11357.

Fritsche-Neto R, Souza TL, Pereira HS, Faria LC, Melo LC, Novaes E, Brum IJ and Jannink JL (2019) Association mapping in common bean revealed regions associated with anthracnose and angular leaf spot resistance. Scientia Agricola 76: 321-7.

Galeano CH, Cortes AJ, Fernández AC, Soler A, Franco-Herrera N, Makunde G, Vanderleyden J and Blair MW (2012) Gene-based single nucleotide polymorphism markers for genetic and association mapping in common bean. BMC genetics 13: 1-1.

Garcia-Fernandez C, Campa A, Garzon AS, Miklas P and Ferreira JJ (2021) GWAS of pod morphological and color characters in common bean. BMC plant biology 21: 1-13.

Gela T, Ramsay L, Haile TA, Vandenberg A and Bett K (2021) Identification of anthracnose race 1 resistance loci in lentil by integrating linkage mapping and genome-wide association study. Plant Genome 14(3): e20131.

Gonçalves-Vidigal MC, Cruz AS, Garcia A, Kami J, Filho PSV, Sousa LL , McClean P, Gepts P and Pastor-Corrales MA (2011) Linkage mapping of the Phg-1 and Co-14 genes for resistance to angular leaf spot and anthracnose in the common bean cultivar AND 277. Theoretical and Applied Genetics 122: 893–903.

Gunjača, J, Carović-Stanko K, Lazarevi, B, Vidak M, Petek M, Liber Z and Šatović Z (2021) Genome-wide association studies of mineral content in common bean. Frontiers in plant science 12: 636484.

Gutiérrez N, Pégard M, Balko C and Torres AM (2023) Genome-wide association analysis for drought tolerance and associated traits in faba bean (Vicia faba L.). Frontiers in Plant Science 14: 1091875.

Han X, Li L, Chen H, Liu L, Sun L, Wang X, Xiang Y, Wan Z and Liu C (2022) Resequencing of 558 Chinese mungbean landraces identifies genetic loci associated with key agronomic traits. Frontiers in Plant Science 13: 1043784.

Hanai LR, Santini L, Camargo LE, Fungaro MH, Gepts P, Tsai SM and Vieira ML (2010) Extension of the core map of common bean with EST-SSR, RGA, AFLP, and putative functional markers. Molecular Breeding 25: 25-45.

Heineck GC, Altendorf KR, Coyne CJ, Ma Y, McGee R and Porter LD (2022) Phenotypic and Genetic Characterization of the Lentil Single Plant-Derived Core Collection for Resistance to Root Rot Caused by Fusarium avenaceum. Phytopathology 112(9): 1979-1987.

Henares BM, Blake SN, Farfan-Caceres L, Tahghighi H, Debler JW, Russ MH, Farquharson EA, Rose JA, Khani M, Davidson J, Kamphuis LG and Lee RC (2023) Virulence profiles and genome-wide association study for Ascochyta lentis isolates collected from Australian lentil-growing regions. Phytopathology.

Hindu V, Palacios-Rojas N, Babu R, Suwarno WB, Rashid Z, Usha R and Nair SK (2018) Identification and validation of genomic regions influencing kernel zinc and iron in maize. Theoretical and Applied Genetics 131: 1443–1457

Howie B, Fuchsberger C, Stephens M, Marchini J and Abecasis GR (2012) Fast and accurate genotype imputation in genome-wide association studies through pre-phasing. Nature Genetics 44(8): 955-959.

Hoyos-Villegas V, Song Q and Kelly JD (2017) Genome-wide association analysis for drought tolerance and associated traits in common bean. Plant Genome 10: 1-17.

Huang M, Liu X, Zhou Y, Summers RM and Zhang Z (2019) BLINK: a package for the next level of genome-wide association studies with both individuals and markers in the millions. Gigascience 8(2): giy154.

Huster AR, Wallace LT and Myers JR (2021) Associated SNPs, Heritabilities, Trait Correlations, and Genomic Breeding Values for Resistance in Snap Beans (Phaseolus vulgaris L.) to Root Rot Caused by Fusarium solani (Mart.) f. sp. phaseoli (Burkholder). Frontiers in Plant Science 12: 697615.

Ibrahim AK, Zhang L, Niyitanga S, Afzal MZ, Xu Y, Zhang L and Qi J (2020) Principles and approaches of association mapping in plant breeding. Tropical Plant Biology 13: 212- 224.

Iriti M and Varoni EM (2017) Pulses, Healthy, and Sustainable Food Sources for Feeding the Planet. International Journal of molecular sciences 18(2): 255.

Jannink JL, Lorenz AJ and Iwata H (2010) Genomic selection in plant breeding: from theory to practice. Briefings in functional genomics 9(2): 166-177.

Jha UC, Jha R, Thakro V, Kumar A, Gupta S, Nayyar H, Basu P, Parida SK and Singh NP (2021) Discerning molecular diversity and association mapping for phenological, physiological and yield traits under high temperature stress in chickpea (Cicer arietinum L.). Journal of Genetics 100: 1-5.

Jiang W, Zhang X, Li S, Song S and Zhao H (2022) An unbiased kinship estimation method for genetic data analysis. BMC bioinformatics 23(1): 1-22.

Johnson N, Boatwright JL, Bridges W, Thavarajah P, Kumar S, Shipe E and Thavarajah D (2021) Genome-wide association mapping of lentil (Lens culinaris Medikus) prebiotic carbohydrates toward improved human health and crop stress tolerance. Scientific Reports 11(1): 13926.

Kaler AS and Purcell LC (2019) Estimation of a significance threshold for genome-wide association studies. BMC Genomics 20: 618.

Kalve S, Gali KK and Taran B (2022) Genome-wide association analysis of stress tolerance indices in an interspecific population of chickpea. Frontiers in Plant Science 13: 933277.

Kamfwa K, Cichy KA and Kelly JD (2015a) Genome‐wide association study of agronomic traits in common bean. The Plant Genome 8(2): 2014-09.

Kamfwa K, Cichy KA and Kelly JD (2015b) Genome-wide association analysis of symbiotic nitrogen fixation in common bean. Theoretical and Applied Genetics 128: 1999- 2017.

Katoch V, Sharma S, Pathania S, Banyal D, Sharma S and Rathour R (2010) Molecular mapping of pea powdery mildew resistance gene er2 to pea linkage group III. Molecular Breeding 25: 229-237.

Katuuramu DN, Hart JP, Porch TG, Grusak MA, Glahn RP and Cichy KA (2018) Genome- wide association analysis of nutritional composition-related traits and iron bioavailability in cooked dry beans (Phaseolus vulgaris L.). Molecular Breeding 38: 44.

Kaur S, Cogan N O, Stephens A, Noy D, Butsch M, Forster J W and Materne M (2014) EST- SNP discovery and dense genetic mapping in lentil (Lens culinaris Medik.) enable candidate gene selection for boron tolerance. Theoretical and Applied Genetics 127: 703-713.

Kinhoegbe G, Djedatin G, Saxena RK, Chitikineni A, Bajaj P, Molla J, Agbangla C, Dansi A, and Varshney RK (2022) Genetic diversity and population structure of pigeonpea (Cajanus cajan [L.] Millspaugh) landraces grown in Benin revealed by Genotyping- By- Sequencing. Plos one 17(7): e0271565.

Klein RJ, Zeiss C, Chew EY, Tsai JY, Sackler RS, Haynes C and Bracken MB (2005) Complement factor H polymorphism in age-related macular degeneration. Science 308: 385–389.

Korte A and Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9: 29.

Kumar K, Anjoy P, Sahu S, Durgesh K, Das A, Tribhuvan KU, Sevanthi AM, Joshi R, Jain PK, Singh NK, Rao AR and Gaikwad K (2022) Single trait versus principal component based association analysis for flowering related traits in pigeonpea. Scientific Reports 12(1): 10453.

Kumar N, Bharadwaj C, Sahu S, Shiv A, Shrivastava AK, Reddy SPP, Soren KR, Patil BS, Pal M, Soni A, Roorkiwal M and Varshney RK (2021) Genome-wide identification and functional prediction of salt- stress related long non-coding RNAs (lncRNAs) in chickpea (Cicer arietinum L.). Physiology and Molecular Biology of Plants 27(11): 2605-2619.

Kumar K, Kumar M, Kim SR, Ryu H and Cho YG (2013) Insights into genomics of salt stress response in rice. Rice 6(1): 1-5.

Kumari G, Shanmugavadivel PS, Lavanya GR, Tiwari P, Singh D, Gore PG, Tripathi K, Madhavan Nair R, Gupta S and Pratap A (2022) Association mapping for important agronomic traits in wild and cultivated Vigna species using cross-species and cross- genera simple sequence repeat markers. Frontiers in Genetics 13: 1000440.

Langyan S, Yadava P, Khan FN, Bhardwaj R, Tripathi K, Bhardwaj V, Bhardwaj R, Gautam RK and Kumar A (2022) Nutritional and food composition survey of major pulses toward healthy, sustainable, and biofortified diets. Frontiers in Sustainable Food Systems 6: 878269.

Leonforte A, Sudheesh S, Cogan NO, Salisbury PA, Nicolas ME, Materne M, Forster JW and Kaur S (2013) SNP marker discovery, linkage map construction and identification of QTLs for enhanced salinity tolerance in field pea (Pisum sativum L.). BMC Plant Biology 13: 161.

Li M, Wu X, Wang B, Wu X, Wang Y, Wang J, Dong J, Wu J, Lu Z, Sun Y, Dong W, Yang J and Li G (2023) Genome-wide association analysis reveals the optimal genomic regions for pod size in bean. Frontiers in Plant Science 14: 1138988.

Li Y, Ruperao P, Batley J, Edwards D, Davidson J, Hobson K and Sutton T (2017) Genome Analysis Identified Novel Candidate Genes for Ascochyta Blight Resistance in Chickpea Using Whole Genome Re-sequencing Data. Frontiers in Plant Science 8: 359.

Li Y, Ruperao P, Batley J, Edwards D, Khan T, Colmer TD, Pang J, Siddique KH and Sutton T (2018) Investigating drought tolerance in chickpea using genome-wide association mapping and genomic selection based on whole-genome resequencing data. Frontiers in Plant Science 9: 190.

Liu J, Xue C, Lin Y, Yan Q, Chen J, Wu R, Zhang X, Chen X and Yuan X (2022) Genetic analysis and identification of VrFRO8, a salt tolerance-related gene in mungbean. Gene 836: 146658.

Liu X, Huang M, Fan B, Buckler ES and Zhang Z (2016) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS genetics 12(2): e1005767.

Liu Z, Gao S, Zhang H, Xu Z and Qian W (2022) Genome-Wide Association Study Reveals That PvGUX1_1 Is associated with Pod Stringlessness in Snap Bean (Phaseolus vulgaris L.). Biology (Basel) 11(4): 611.

Liu Z, Zhu C, Jiang Y, Tian Y, Yu J, An H, Tang W, Sun J, Tang J, Chen G, Zhai H, Wang C and Wan J (2016) Association mapping and genetic dissection of nitrogen use efficiency-related traits in rice (Oryza sativa L.) Functional and Integrative Genomics 16 (3): 323-333.

Lo S, Muñoz-Amatriaín M, Hokin SA, Cisse N, Roberts PA, Farmer AD, Xu S and Close TJ (2019) A genome-wide association and meta-analysis reveal regions associated with seed size in cowpea [Vigna unguiculata (L.) Walp]. Theoretical and Applied Genetics 132(11): 3079-3087.

Lv C, Lu W, Quan M, Xiao L, Li L, Zhou J, Li P, Zhang D and Du Q (2021) Pyramiding superior haplotypes and epistatic alleles to accelerate wood quality and yield improvement in poplar breeding. Industrial Crops and Products 171: 113891.

Ma Y, Marzougui A, Coyne CJ, Sankaran S, Main D, Porter LD, Mugabe D, Smitchger JA, Zhang C, Amin MN, Rasheed N, Ficklin SP and McGee RJ (2020) Dissecting the Genetic Architecture of Aphanomyces root rot resistance in Lentil by QTL Mapping and Genome-Wide Association Study. International Journal of Molecular Sciences 21(6): 2129.

Maalouf F, Abou-Khater L, Babiker Z, Jighly A, Alsamman AM, Hu J, Ma Y, Rispail N, Balech R, Hamweih A, Baum M and Kumar S (2022) Genetic Dissection of Heat Stress Tolerance in Faba Bean (Vicia faba L.) using GWAS. Plants (Basel) 11(9): 1108.

Mahajan R, Zargar SM, Salgotra RK, Singh R, Wani AA, Nazir M and Sofi PA (2017) Linkage disequilibrium based association mapping of micronutrients in common bean (Phaseolus vulgaris L.): a collection of Jammu & Kashmir, India. 3 Biotech 7: 1-3.

Mandel JR, Nambeesan S, Bowers JE, Marek LF, Ebert D, Rieseberg LH, Knapp SJ and Burke JM (2013) Association mapping and the genomic consequences of selection in sunflower. PLoS Genetetics 9: e1003378.

Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A and Cho JH (2009) Finding the missing heritability of complex diseases. Nature 461(7265):747-53.

Metternicht GI and Zinck JA (2003) Remote sensing of soil salinity: potentials and constraints. Remote sensing of Environment 85(1):1-20.

Moghaddam SM, Mamidi S, Osorno JM, Lee R, Brick M, Kelly J, Miklas P, Urrea C, Song Q, Cregan P and Grimwood J (2016) Genome‐wide association study identifies candidate loci underlying agronomic traits in a Middle American diversity panel of common bean. The Plant Genome 9(3): 02.

Morton MJL, Awlia M, Al-Tamimi N, Saade S, Pailles Y, Negrào S and Tester M (2019) Salt stress under the scalpel-Dissecting the genetics of salt tolerance. The Plant Journal 97: 148-163.

Munns R and Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59: 651-81.

Myers JR, Wallace T, Mafi Moghaddam S, Kleintop AE, Echeverria D, Thompson HJ, Brick MA, Lee R and McClean PE (2019) Improving the health benefits of snap bean: genome-wide association studies of total phenolic content. Nutrients 11(10): 2509.

Nascimento M, Nascimento AC, Silva FF, Barili LD, Vale NM, Carneiro JE, Cruz CD, Carneiro PC and Serao NV (2018) Quantile regression for genome-wide association study of flowering time-related traits in common bean. PLoS One 13(1): e0190303.

Nemli S, Asciogul TK, Kaya HB, Kahraman A, Eşiyok D and Tanyolac B (2014) Association mapping for five agronomic traits in the common bean (Phaseolus vulgaris L.). Journal of the Science of Food and Agriculture 41: 389-404.

Neupane S, Wright DM, Martinez RO, Butler J, Weller JL and Bett KE (2023) Focusing the GWAS Lens on days to flower using latent variable phenotypes derived from global multienvironment trials. The Plant Genome 16(1): e20269.

Nkhata W, Shimelis H, Melis R, Chirwa R, Mzengeza T, Mathew I and Shayanowako A (2021) Genome-wide association analysis of bean fly resistance and agro- morphological traits in common bean. PLoS One 16(4): e0250729.

Noble TJ, Tao Y, Mace ES, Williams B, Jordan DR, Douglas CA and Mundree SG (2018) Characterization of linkage disequilibrium and population structure in a mungbean diversity panel. Frontiers in Plant Science 8: 2102.

Nordborg M and Weigel D (2008) Next-generation genetics in plants. Nature 456:720.

Ojwang PP, Eldridge T, Corredor-Moreno P and Njunge V (2021) Structure of genetic diversity and genome-wide association studies of bean fly (Ophiomyia spencerella) resistance in common bean. Euphytica 217: 1-21.

Oladzad A, Porch T, Rosas JC, Moghaddam SM, Beaver J, Beebe SE, Burridge J, Jochua C N, Miguel MA, Miklas PN and Ratz B (2019) Single and multi-trait GWAS identify genetic factors associated with production traits in common bean under abiotic stress environments. G3: Genes, Genomes, Genetics 9(6):1881-92.

Ongom PO, Togola A, Fatokun C and Boukar O (2022) A Genome-Wide Scan Divulges Key Loci Involved in Resistance to Aphids (Aphis craccivora) in Cowpea (Vigna unguiculata). Genes (Basel) 13(11): 2002.

Patil PG, Dubey J, Bohra A, Mishra RK, Saabale PR, Das A, Rathore M and Singh NP (2017) Association mapping to discover significant marker-trait associations for resistance against Fusarium wilt variant 2 in pigeonpea [Cajanus cajan (L.) Millspaugh] using SSR markers. Journal of Applied Genetics 58: 307-19.

Paudel D, Dareus R, Rosenwald J, Munoz-Amatriaín M and Rios EF (2021) Genome-Wide Association Study Reveals Candidate Genes for Flowering Time in Cowpea (Vigna unguiculata [L.] Walp.). Frontiers in Genetics 12: 667038.

Perseguini JM, Oblessuc PR, Rosa JR, Gomes KA, Chiorato AF, Carbonell SA, Garcia AA, Vianello RP and Benchimol-Reis LL (2016) Genome-wide association studies of anthracnose and angular leaf spot resistance in common bean (Phaseolus vulgaris L.). PLoS One 11(3): e0150506.

Polanco C, Saenz de Miera LE, Gonzalez AI, Garcia P, Fratini R, Vaquero F, Vences FJ and Perez de la Vega M (2019) Construction of a high-density interspecific (Lens culinaris x L. odemensis) genetic map based on functional markers for mapping morphological and agronomical traits, and QTLs affecting resistance to Ascochyta in lentil. PLoS One 14: e0214409.

Pratap A, Chaturvedi SK, Tomar R, Rajan N, Malviya N, Thudi M, Saabale PR, Prajapati U, Varshney RK and Singh NP (2017) Marker-assisted introgression of resistance to fusarium wilt race 2 in Pusa 256, an elite cultivar of desi chickpea. Molecular Genetics and Genomics 292: 1237-1245.

Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA and Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics 38: 904.

Pritchard JK, Stephens M and Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, De Bakker PI, Daly MJ and Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. The American journal of human genetics 81(3): 559-75.

Qian L, Hickey LT, Stahl A, Werner CR, Hayes B, Snowdon RJ and Voss-Fels KP (2017) Exploring and harnessing haplotype diversity to improve yield stability in crops. Frontiers in plant science 8: 1534.

Raggi L, Caproni L, Carboni A and Negri V (2019) Genome-wide association study reveals candidate genes for flowering time variation in common bean (Phaseolus vulgaris L.). Frontiers in plant science 10: 962.

Rahman MA, Kang S, Nagabhatla N and Macnee R (2017) Impacts of temperature and rainfall variation on rice productivity in major ecosystems of Bangladesh. Agriculture & Food Security 6: 1-11.

Rajendran K, Coyne CJ, Zheng P, Saha G, Main D, Amin N, Ma Y, Kisha T, Bett KE, McGee RJ and Kumar S (2021) Genetic diversity and GWAS of agronomic traits using an ICARDA lentil (Lens culinaris Medik.) Reference Plus collection. Plant Genetic Resources 19(4): 279-88.

Raman R, Warren A, Krysinska-Kaczmarek M, Rohan M, Sharma N, Dron N, Davidson J, Moore K and Hobson K (2022) Genome-Wide Association Analyses Track Genomic Regions for Resistance to Ascochyta rabiei in Australian Chickpea Breeding Germplasm. Frontiers in Plant Science 13: 877266.

Rau D, Murgia ML, Rodriguez M, Bitocchi E, Bellucci E, Fois D, Albani D, Nanni L, Gioia T, Santo D and Marcolungo L (2019) Genomic dissection of pod shattering in common bean: mutations at non‐orthologous loci at the basis of convergent phenotypic evolution under domestication of leguminous species. The Plant Journal 97(4): 693-714.

Ravelombola W, Shi A and Huynh BL (2021) Loci discovery, network-guided approach, and genomic prediction for drought tolerance index in a multi-parent advanced generation intercross (MAGIC) cowpea population. Horticulture Research 8(1): 24.

Ravelombola W, Shi A, Huynh BL, Qin J, Xiong H, Manley A, Dong L, Olaoye D, Bhattarai G, Zia B, Alshaya H and Alatawi I (2022) Genetic architecture of salt tolerance in a Multi-Parent Advanced Generation Inter-Cross (MAGIC) cowpea population. BMC Genomics 23(1): 100.

Reddy VR, Das S, Dikshit HK, Mishra GP, Aski M, Meena SK, Singh A, Pandey R, Singh MP, Tripathi K and Gore PG (2020) Genome-wide association analysis for phosphorus use efficiency traits in mungbean (Vigna radiata L. Wilczek) using genotyping by sequencing approach. Frontiers in plant science 11: 537766.

Resende RT, de Resende MD, Azevedo CF, Fonseca e Silva F, Melo LC, Pereira HS, Souza TL, Valdisser PA, Brondani C and Vianello RP (2018) Genome-wide association and regional heritability mapping of plant architecture, lodging and productivity in Phaseolus vulgaris. G3: Genes, Genomes, Genetics 8(8): 2841-54.

Ritchie H, Reay DS and Higgins P (2018) Quantifying, projecting, and addressing India’s hidden hunger. Frontiers in sustainable food systems 2: 11.

Roorkiwal M, Bhandari A, Barmukh R, Bajaj P, Valluri VK, Chitikineni A, Pandey S, Chellapilla B, Siddique KH and Varshney RK (2022) Genome-wide association mapping of nutritional traits for designing superior chickpea varieties. Frontiers in Plant Science 13: 843911.

Sallam A, Arbaoui M, El-Esawi M, Abshire N and Martsch R (2016) Identification and Verification of QTL Associated with Frost Tolerance Using Linkage Mapping and GWAS in Winter Faba Bean. Frontiers in Plant Science 7: 1098.

Sallam A, Moursi YS, Martsch R and Eltaher S (2022) Genome-wide association mapping for root traits associated with frost tolerance in faba beans using KASP-SNP markers. Frontiers in Genetics 13: 907267.

Samineni S, Mahendrakar MD, Hotti A, Chand U, Rathore A and Gaur PM (2022) Impact of heat and drought stresses on grain nutrient content in chickpea: Genome-wide marker-trait associations for protein, Fe and Zn. Environmental and Experimental Botany 194: 104688.

Sanderson LA, Caron CT, Tan R, Shen Y, Liu R and Bett KE (2019) KnowPulse: a web- resource focused on diversity data for pulse crop improvement. Frontiers in Plant Science 10: 965.

Saxena MS, Bajaj D, Kujur A, Das S, Badoni S, Kumar V, Singh M, Bansal KC, Tyagi AK and Parida SK (2014) Natural allelic diversity, genetic structure and linkage disequilibrium pattern in wild chickpea. PLoS One 9(9): e107484.

Segura V, Vilhjálmsson BJ, Platt A, Korte A, Seren Ü, Long Q and Nordborg M (2012) An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations. Nature genetics 44(7): 825-30.

Seo H, Kwon H, Satyawan D, Kim MY, Ha J and Lee SH (2023) Identification of novel loci for flowering time in mungbean [Vigna radiata (L.) R. Wilczek] using genome-wide association study. Genes and Genomics 18: 1-9.

Setakis E, Stirnadel H and Balding DJ (2006) Logistic regression protects against population structure in genetic association studies. Genome Research 16(2): 290–296.

Shi C, Navabi A and Yu K (2011) Association mapping of common bacterial blight resistance QTL in Ontario bean breeding populations. BMC Plant Biology 11: 52.

Singh A, Sharma V, Dikshit HK, Aski M, Kumar H, Thirunavukkarasu N, Patil BS, Kumar S and Sarker A (2017) Association mapping unveils favorable alleles for grain iron and zinc concentrations in lentil (Lens culinaris subsp. culinaris). PLoS One 12(11): e0188296.

Singh B, Singh S, Mahato AK, Dikshit HK, Tripathi K and Bhatia S (2023) Delineation of novel genomic loci and putative candidate genes associated with seed iron and zinc content in lentil (Lens culinaris Medik.). Plant Science 335: 111787.

Singh CM, Pratap A, Gupta S, Biradar RS and Singh NP (2020) Association mapping for mungbean yellow mosaic India virus resistance in mungbean (Vigna radiata L. Wilczek). 3 Biotech 10: 1-2.

Singh D, Singh C, Tomar R S, Karwa S, Singh M P, Singh V, Sanwal S and Sharma P (2020) Genetics and molecular mapping for salinity stress tolerance at seedling stage in lentil (Lens culinaris Medik). Crop Science 60: 1254-1266.

Singh D, Singh CK, Kumari S, Singh Tomar RS, Karwa S, Singh R, Singh RB, Sarkar SK and Pal M (2017) Discerning morpho-anatomical, physiological and molecular multiformity in cultivated and wild genotypes of lentil with reconciliation to salinity stress. PLoS One 12(5): e0177465.

Singh D, Singh CK, Tomar RS, Sharma S, Karwa S, Pal M, Singh V, Sanwal SK and Sharma PC (2020) Genetics and molecular mapping for salinity stress tolerance at seedling stage in lentil (Lens culinaris Medik). Crop Science 60(3):1254-66.

Singh J, Sharma PC, Sharma SK and Rai M (2014) Assessing the effect of salinity on the oil quality parameters of Indian mustard (Brassica juncea L. Czern & Coss) using Fourier Transform Near-Infrared Reflectance (FT-NIR) spectroscopy. Grasas y Aceites 65(1): e009.

Singh L, Dhillon GS, Kaur S, Dhaliwal SK, Kaur A, Malik P, Kumar A, Gill RK and Kaur S (2022) Genome-wide Association Study for Yield and Yield-Related Traits in Diverse Blackgram Panel (Vigna mungo L. Hepper) Reveals Novel Putative Alleles for Future Breeding Programs. Frontiers in Genetics 13: 849016.

Sinha MK, Aski MS, Mishra GP, Kumar MB, Yadav PS, Tokas JP, Gupta S, Pratap A, Kumar S, Nair RM and Schafleitner R (2023) Genome wide association analysis for grain micronutrients and anti-nutritional traits in mungbean [Vigna radiata (L.) R. Wilczek] using SNP markers. Frontiers in Nutrition 10: 1099004.

Sinha P, Singh VK, Saxena RK, Kale SM, Li Y, Garg V, Meifang T, Khan AW, Kim KD, Chitikineni A and Saxena KB (2020) Genome‐wide analysis of epigenetic and transcriptional changes associated with heterosis in pigeonpea. Plant Biotechnology Journal 18(8): 1697-710.

Sodedji FA, Agbahoungba S, Agoyi EE, Kafoutchoni MK, Choi J, Nguetta SP, Assogbadjo AE and Kim HY (2021) Diversity, population structure, and linkage disequilibrium among cowpea accessions. The Plant Genome 14(3): e20113.

Sokolkova A, Burlyaeva M, Valiannikova T, Vishnyakova M, Schafleitner R, Lee CR, Ting CT, Nair RM, Nuzhdin S, Samsonova M and von Wettberg E (2020) Genome-wide association study in accessions of the mini-core collection of mungbean (Vigna radiata) from the World Vegetable Gene Bank (Taiwan). BMC plant biology 20: 1-9.

Soler-Garzón A, Goldoff D, Thornton A, Swisher Grimm KD, Hart JP, Song Q, Strausbaugh CA and Miklas PN (2023) A robust SNP-haplotype assay for Bct gene region conferring resistance to beet curly top virus in common bean (Phaseolus vulgaris L.). Frontiers in Plant Science 14: 1215950.

Soltani A, MafiMoghaddam S, Oladzad-Abbasabadi A, Walter K, Kearns PJ, Vasquez- Guzman J, Mamidi S, Lee R, Shade AL, Jacobs JL and Chilivers MI (2018) Genetic analysis of flooding tolerance in an Andean diversity panel of dry bean (Phaseolus vulgaris L.). Frontiers in plant science 9: 767.

Soltani A, MafiMoghaddam S, Walter K, Restrepo-Montoya D, Mamidi S, Schroder S, Lee R, McClean PE and Osorno JM (2017) Genetic architecture of flooding tolerance in the dry bean Middle-American diversity panel. Frontiers in plant science 8: 1183.

Srungarapu R, Mahendrakar MD, Mohammad LA, Chand U, Jagarlamudi VR, Kondamudi K P, Kudapa H and Samineni S (2022) Genome-Wide Association Analysis Reveals Trait-Linked Markers for Grain Nutrient and Agronomic Traits in Diverse Set of Chickpea Germplasm. Cells 11(15): 2457.

Sun Z, Li H, Zhang Y, Li Z, Ke H, Wu L, Zhang G, Wang X and Ma Z (2018) Identification of SNPs and candidate genes associated with salt tolerance at the seedling stage in cotton (Gossypium hirsutum L.). Frontiers in Plant Science 9: 1011.

Thudi M, Chen Y, Pang J, Kalavikatte D, Bajaj P, Roorkiwal M, Chitikineni A, Ryan MH, Lambers H, Siddique KHM and Varshney RK (2021) Novel Genes and Genetic Loci Associated With Root Morphological Traits, Phosphorus-Acquisition Efficiency and Phosphorus-Use Efficiency in Chickpea. Frontiers in Plant Science 12: 636973.

Thudi M, Upadhyaya HD, Rathore A, Gaur PM, Krishnamurthy L, Roorkiwal M, Nayak SN, Chaturvedi SK, Basu PS, Gangarao NV and Fikre A (2014) Genetic dissection of drought and heat tolerance in chickpea through genome-wide and candidate gene- based association mapping approaches. Plos one 9(5): e96758.

Tock AJ, Fourie D, Walley PG, Holub EB, Soler A, Cichy KA, Pastor-Corrales MA, Song Q, Porch TG, Hart JP and Vasconcellos RC (2017) Genome-wide linkage and association mapping of halo blight resistance in common bean to race 6 of the globally important bacterial pathogen. Frontiers in Plant Science 8: 1170.

Ugwuanyi S, Udengwu OS, Snowdon RJ and Obermeier C (2022) Novel candidate loci for morpho-agronomic and seed quality traits detected by targeted genotyping-by- sequencing in common bean. Frontiers in Plant Science 13: 1014282.

Upadhyaya HD, Bajaj D, Narnoliya L, Das S, Kumar V, Gowda CL, Sharma S, Tyagi AK and Parida SK (2016) Genome-wide scans for delineation of candidate genes regulating seed-protein content in chickpea. Frontiers in Plant Science 7: 302.

Varshney RK, Mohan SM, Gaur PM, Chamarthi SK, Singh VK, Srinivasan S, Swapna M, Sharma S, Pande S, Singh S and Kaur L (2014) Marker-assisted backcrossing to introgress resistance to Fusarium wilt race 1 and Ascochyta blight in C 214, an elite cultivar of chickpea. The Plant Genome 7: 1-11.

Varshney RK, Mohan SM, Gaur PM, Gangarao NV, Pandey MK, Bohra A, Sawargaonkar SL, Chitikineni A, Kimurto PK, Janila P and Saxena KB (2013) Achievements and prospects of genomics-assisted breeding in three legume crops of the semi-arid tropics. Biotechnology advances 31(8): 1120-34.

Vasconcellos RC, Oraguzie OB, Soler A, Arkwazee H, Myers JR, Ferreira JJ, Song Q, McClean P and Miklas PN (2017) Meta-QTL for resistance to white mold in common bean. PLoS One 12: e0171685.

Vilhjalmsson BJ and Nordborg M (2013) The nature of confounding in genome-wide association studies. Nature Review Genetics 14(1): 1-2.

Visscher PM, Wray NR, Zhang Q, Sklar P, McCarthy MI, Brown MA and Yang J (2017) 10 years of GWAS discovery: biology, function, and translation. The American Journal of Human Genetics 101(1): 5-22.

Wang WY, Barratt BJ, Clayton DG and Todd JA (2005) Genome-wide association studies: theoretical and practical concerns. Nature Reviews Genetics 6(2): 109-18.

Wigginton JE, Cutler DJ and Abecasis GR (2005) A note on exact tests of Hardy-Weinberg equilibrium. American Journal of Human Genetics 76(1): 887-893.

Wu L, Fredua-Agyeman R, Hwang SF, Chang KF, Conner RL, McLaren DL and Strelkov S E (2021) Mapping QTL associated with partial resistance to Aphanomyces root rot in pea (Pisum sativum L.) using a 13.2 K SNP array and SSR markers. Theoretical and Applied Genetics 134: 2965-2990.

Wu X, Wang B, Xin Y, Wang Y, Tian S, Wang J, Wu X, Lu Z, Qi X, Xu L and Li G (2022) Unravelling the Genetic Architecture of Rust Resistance in the Common Bean (Phaseolus vulgaris L.) by Combining QTL-Seq and GWAS Analysis. Plants (Basel). 11(7): 953.

Xu N, Chen B, Cheng Y, Su Y, Song M, Guo R, Wang M, Deng K, Lan T, Bao S, Wang G, Guo Z and Yu L (2023) Integration of GWAS and RNA-Seq Analysis to Identify SNPs and Candidate Genes Associated with Alkali Stress Tolerance at the Germination Stage in Mung Bean. Genes (Basel). 14(6): 1294.

Xu Y, Li P, Yang Z and Xu C (2017) Genetic mapping of quantitative trait loci in crops. Crop Journal 5: 175-184.

Zeng P, Zhao Y, Qian C, Zhang L, Zhang R, Gou J, Liu J, Liu L and Chen F (2015) Statistical analysis for genome-wide association study. Journal of biomedical research 29(4): 285.

Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM and Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nature genetics 42(4): 355-60.

Zhao J, Bayer PE, Ruperao P, Saxena RK, Khan AW, Golicz AA, Nguyen HT, Batley J, Edwards D and Varshney RK (2020) Trait associations in the pangenome of pigeon pea (Cajanus cajan). Plant biotechnology journal 18(9): 1946-54.

Zhao K, Aranzana MJ, Kim S, Lister C, Shindo C, Tang C, Toomajian C, Zheng H, Dean C, Marjoram P and Nordborg M (2007) An Arabidopsis example of association mapping in structured samples. PLoS genetics 3(1): e4.

Zuiderveen GH, Padder BA, Kamfwa K, Song Q and Kelly JD (2016) Genome-Wide association study of anthracnose resistance in andean beans (Phaseolus vulgaris). PLoS One 11: e156391.

Downloads

Submitted

2023-08-28

Published

2023-12-31

Issue

Section

Review Article

How to Cite

Shekhawat, P. K. ., Singh, J. ., Jakhar, M. L. ., Punia, S. S. ., & Singh, V. . (2023). Genome Wide Association Study in Pulses for Salt Tolerance: Status and Perspective. Journal of Soil Salinity and Water Quality, 15(2), 127-145. https://epubs.icar.org.in/index.php/JoSSWQ/article/view/141587