Abstract
Stemphylium blight caused by Stemphylium botryosum, is a foliar disease of lentil. It affects the productivity and milling quality of lentil crops, mainly in South Asia and Canada. Development of stemphylium blight resistant cultivars by introgression of resistance alleles from crop wild relatives of lentil, such as Lens ervoides, is one strategy of disease control. The objective of this study was to identify genomic regions associated with stemphylium blight resistance by combining linkage mapping and marker-trait association analysis. A total of 182 genotypes of a lentil advanced backcross population (LABC-01) developed from the backcross of the interspecific L. culinaris × L. ervoides line LR-59-81 (donor) and cultivar CDC Redberry (recurrent) and 101 diverse lentil accessions selected by stratified random sampling from a lentil diversity panel were genotyped and evaluated for stemphylium blight reactions. Quantitative trait locus (QTL) analysis identified four loci contributing to stemphylium blight resistance on lentil chromosomes 2, 4 and 5. Marker trait association analysis detected five significant single nucleotide polymorphism (SNP) markers associated with stemphylium blight resistance within QTLs regions and seven SNP markers outside the QTLs regions on chromosomes 1, 2, 3, 5, and 7. The markers associated with stemphylium blight resistance may be useful for marker-assisted selection of resistant cultivars after validation.
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Data availability
The raw genotypic datasets analyzed and presented in the current study are available at https://knowpulse.usask.ca upon request from the corresponding author.
References
Adobor S, Podder R, Banniza S, Vandenberg A (2020) Evaluation of resistance to stemphylium blight in interspecific recombinant inbred lines derived from Lens culinaris × Lens ervoides. Plant Genetic Resour Charact Util 18:251–258. https://doi.org/10.1017/S1479262120000295
Afzal AJ, Wood AJ, Lightfoot DA (2008) Plant receptor-like serine threonine kinases: roles in signaling and plant defense. Mol Plant Microbe Interact 21:507–517. https://doi.org/10.1094/MPMI-21-5-0507
Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–218. https://doi.org/10.1007/BF02672069
Bauer AM, Hoti F, Von Korff M, Pillen K, Léon J, Sillanpää MJ (2009) Advanced backcross-QTL analysis in spring barley (H. vulgare ssp. spontaneum) comparing a REML versus a Bayesian model in multi-environmental field trials. Theor Appl Genet 119:105–123. https://doi.org/10.1007/s00122-009-1021-6
Bayaa B, Erskine W (1998) Diseases of lentil. In: Allen DJ, Lenne JM (Ed) The Pathology of Food and Pasture Legumes. Wallingford: CAB International in association with the International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), pp 442–443.
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc: Ser B (Methodol) 57:289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Bhadauria V, Ramsay L, Bett KE, Banniza S (2017) QTL mapping reveals genetic determinants of fungal disease resistance in the wild lentil species Lens ervoides. Sci Rep 7:1–9. https://doi.org/10.1038/s41598-017-03463-9
Borevitz JO, Nordborg M (2003) The impact of genomics on the study of natural variation in Arabidopsis. Plant Physiol 132:718–725. https://doi.org/10.1104/pp.103.023549
Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M et al (2010) Linkage and association mapping of Arabidopsis thaliana flowering time in Nature. PLoS Genetics 6:e1000940. https://doi.org/10.1371/journal.pgen.1000940
Campos MD, Félix MDR, Patanita M, Materatski P, Albuquerque A, Ribeiro JA et al (2022) Defense strategies: the role of transcription factors in tomato–pathogen interaction. Biology 11:235. https://doi.org/10.3390/biology11020235
Chen L-A (2018) Assessing the impacts of crop-wild introgression in lentil using interspecific Lens species recombinant inbred line populations. PhD Dissertation, University of Saskatchewan
Chen J, Shrestha R, Ding J, Zheng H, Mu C, Wu J et al (2016) Genome-wide association study and QTL mapping reveal genomic loci associated with fusarium ear rot resistance in tropical maize germplasm. G3 Genes Genomes Genetics 6:3803–3815. https://doi.org/10.1534/g3.116.034561
Collard BCY, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc b Biol Sci 363:557–572. https://doi.org/10.1098/rstb.2007.2170
Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142:169–196. https://doi.org/10.1007/s10681-005-1681-5
Corwin JA, Kliebenstein DJ (2017) Quantitative resistance: more than just perception of a pathogen. Plant Cell 29:655–665. https://doi.org/10.1105/tpc.16.00915
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA et al (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158. https://doi.org/10.1093/bioinformatics/btr330
El-Soda M, Malosetti M, Zwaan BJ, Koornneef M, Aarts MGM (2014) Genotype × environment interaction QTL mapping in plants: lessons from Arabidopsis. Trends Plant Sci 19:390–398. https://doi.org/10.1016/j.tplants.2014.01.001
Erskine W, Sarker A (1996) Lentil: the Bangladesh breakthrough. ICARDA Caravan 6:8–9
FAOSTAT (2020) Food and Agriculture Organization of the United Nations (FAO). FAOSTAT Database. Rome, Italy. Retrieved March 14, 2020
Fiala JV, Tullu A, Banniza S, Ginette SS, Vandenberg A (2009) Interspecies transfer of resistance to anthracnose in lentil (Lens culinaris medic.). Crop Sci 49:825–830. https://doi.org/10.2135/cropsci2008.05.0260
Ford-Lloyd BV, Schmidt M, Armstrong SJ, Barazani O, Engels J, Hadas R et al (2011) Crop wild relatives-undervalued, underutilized and under threat? Bioscience 61:559–565. https://doi.org/10.1525/bio.2011.61.7.10
Frary A, Fulton TM, Zamir D, Tanksley SD (2004) Advanced backcross QTL analysis of a Lycopersicon esculentum × L. pennellii cross and identification of possible orthologs in the Solanaceae. Theor Appl Genet 108:485–496. https://doi.org/10.1007/s00122-003-1422-x
Gela TS (2021) Mapping and analysis of genetic loci conferring resistance to anthracnose in lentil. PhD Dissertation, University of Saskatchewan
Gela TS, Banniza S, Vandenberg A (2020) Lack of effective resistance to the virulent race of Colletotrichum lentis in Lens culinaris Medikus subsp. culinaris. Plant Genetic Resour Charact Util 18:81–87. https://doi.org/10.1017/S1479262120000027
Gela TS, Koh CS, Caron CT, Chen L, Vandenberg A, Bett KE (2021a) QTL mapping of lentil anthracnose (Colletotrichum lentis) resistance from Lens ervoides accession IG 72815 in an interspecific RIL population. Euphytica 217:70. https://doi.org/10.1007/s10681-021-02804-0
Gela TS, Adobor S, Khazaei H, Vandenberg A (2021) An advanced lentil backcross population developed from a cross between Lens culinaris × L. ervoides for future disease resistance and genomic studies. Plant Genetic Resour Charact Util. https://doi.org/10.1017/S1479262121000216
Gela TS, Ramsay L, Haile TA, Vandenberg A, Bett KE (2021) Identification of anthracnose race 1 resistance loci in lentil by integrating linkage mapping and genome-wide association study. The Plant Genome. https://doi.org/10.1007/s10681-021-02804-0
Haile TA, Heidecker T, Wright D, Neupane S, Ramsay L, Vandenberg A et al (2020) Genomic selection for lentil breeding: Empirical evidence. Plant Genome 13:e20002. https://doi.org/10.1002/TPG2.20002
Hajjar R, Hodgkin T (2007) The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica 156:1–13. https://doi.org/10.1007/s10681-007-9363-0
Hamel LP, Nicole MC, Duplessis S, Ellis BE (2012) Mitogen-activated protein kinase signaling in plant-interacting fungi: distinct messages from conserved messengers. Plant Cell 24:1327–1351. https://doi.org/10.1105/tpc.112.096156
Han Y, Li D, Zhu D, Li H, Li X, Teng W et al (2012) QTL analysis of soybean seed weight across multi-genetic backgrounds and environments. Theor Appl Genet 125:671–683. https://doi.org/10.1007/s00122-012-1859-x
Haussmann BIG, Parzies HK, Presterl T, Susic Z, Miedaner T (2004) Plant genetic resources in crop improvement. Plant Genetic Resour Charact Util 2:3–21. https://doi.org/10.1079/PGR200430
Jiang C, Zhang X, Liu H, Xu JR (2018) Mitogen-activated protein kinase signaling in plant pathogenic fungi. PLoS Pathog 14:4–11. https://doi.org/10.1371/journal.ppat.1006875
Jombart T (2008) Genetics and population analysis adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471-2156-11-94
Khazaei H, Subedi M, Nickerson M, Martínez-Villaluenga C, Frias J, Vandenberg A (2019) Seed protein of lentils: current status, progress, and food applications. Foods 8:391. https://doi.org/10.3390/foods8090391
Knapp SJ, Stroup WW, Ross WM (1985) Exact confidence intervals for heritability on a progeny mean basis. Crop Sci 25:192–194. https://doi.org/10.2135/cropsci1985.0011183X002500010046x
Ladizinsky G (1987) Pulse domestication before cultivation. Econ Bot 41:60–65. https://doi.org/10.1007/BF02859349
Liu X, Huang M, Fan B, Buckler ES, Zhang Z (2016) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet 12(2):e1005767. https://doi.org/10.1371/journal.pgen.1005767
Mammadov J, Sun X, Gao Y, Ochsenfeld C, Bakker E, Ren R et al (2015) Combining powers of linkage and association mapping for precise dissection of QTL controlling resistance to gray leaf spot disease in maize (Zea mays L.). BMC Genomics 16:1–16. https://doi.org/10.1186/s12864-015-2171-3
Maxted N, Kell SP, Ford-Lloyd BV (2008) Crop wild relative conservation and use: establishing the context. In: Maxted N, Ford-Lloyd BV, Kell SP, Iriondo JM, Dulloo ME, Turok J (eds) Crop wild relative conservation and use. CABI, Wallingford
McCouch S, Cho Y, Yano M, Paul E, Blinstrub M, Morishima H et al (1997) Report on QTL nomenclature. Rice Genet Newsl 14:11–131
Meng L, Li H, Zhang L, Wang J (2015) QTL IciMapping: Integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. Crop J 3:269–283. https://doi.org/10.1016/j.cj.2015.01.001
Morrall RAA, Vandenberg A, Banniza S (2004) Recent developments in lentil pathology in Canada. In: Proceedings of the 5th Canadian Pulse Research Workshop. London, ON
Morrall RAA, Carriere B, Ernst B, Pearse C, Schmeling D, Thomson L (2006) Seed-borne pathogens of lentil in Saskatchewan in 2005. Can Plant Dis Surv 86:104–105
Mwakutuya E, Banniza S (2010) Influence of temperature and wetness periods on the development of stemphylium blight on lentil. Plant Dis 94:1219–1224. https://doi.org/10.1094/PDIS-12-09-0804
Narasimhamoorthy B, Gill BS, Fritz AK, Nelson JC, Brown-Guedira GL (2006) Advanced backcross QTL analysis of a hard winter wheat × synthetic wheat population. Theor Appl Genet 112:787–796. https://doi.org/10.1007/s00122-005-0159-0
Naz AA, Kunert A, Lind V, Pillen K, Léon J (2008) AB-QTL analysis in winter wheat: II. Genetic analysis of seedling and field resistance against leaf rust in a wheat advanced backcross population. Theor Appl Genet 116:1095–1104. https://doi.org/10.1007/s11032-012-9710-2
Nordborg M, Tavaré S (2002) Linkage disequilibrium: what history has to tell us. Trends Genet 18:83–90. https://doi.org/10.1016/S0168-9525(02)02557-X
Ogutcen E, Ramsay L, von Wettberg EB, Bett KE (2018) Capturing variation in Lens (Fabaceae): development and utility of an exome capture array for lentil. Appl Plant Sci 6:1–12. https://doi.org/10.1002/aps3.1165
Paterson AH, Lander ES, Hewitt JD, Peterson S, Lincoln SE, Tanksley SD (1988) Resolution of quantitative traits into Mendelian factors by using a complete linkage map of restriction fragment length polymorphisms. Nature 335:721–726. https://doi.org/10.1038/335721a0
Podder R, Banniza S, Vandenberg A (2013) Screening of wild and cultivated lentil germplasm for resistance to stemphylium blight. Plant Genet Res 11:26–35. https://doi.org/10.1017/S1479262112000329
Purcell S (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575. https://doi.org/10.1086/519795
R Core Team (2021) R: a language and environment for statistical computing. Vienna, Austria. [Online] Available: https://www.r-project.org
Ramsay L, Koh CS, Kagale S, Gao D, Kaur S, Haile T et al (2021) Genomic rearrangements have consequences for introgression breeding as revealed by genome assemblies of wild and cultivated lentil species. bioRxiv. https://doi.org/10.1101/2021.07.23.453237
Saha GC, Sarker A, Chen W, Vandemark GJ, Muehlbauer FJ (2010) Inheritance and linkage map positions of genes conferring resistance to Stemphylium blight in lentil. Crop Sci 50:1831–1839. https://doi.org/10.2135/cropsci2009.12.0709
Sanderson LA, Caron CT, Tan R, Shen Y, Liu R, Bett KE (2019) KnowPulse: a web-resource focused on diversity data for pulse crop improvement. Front Plant Sci 10:965. https://doi.org/10.3389/fpls.2019.00965
Schmalenbach I, Körber N, Pillen K (2008) Selecting a set of wild barley introgression lines and verification of QTL effects for resistance to powdery mildew and leaf rust. Theor Appl Genet 117:1093–1106. https://doi.org/10.1007/s00122-008-0847-7
Silvana G, Tanksley SD (2005) Advanced backcross QTL analysis: results and perspectives. In: Tuberosa R, Phillips RL, and Gale M (Ed) Proceedings of the International Congress “In the Wake of the Double Helix: From the Green Revolution to the Gene Revolution”, 27–31 May 2003. Avenue Media: Bologna, Italy, pp. 115–132
Slinkard AE (1981) Eston lentil. Can J Plant Sci 61:733–734. https://doi.org/10.4141/cjps81-104
Stam P, Zeven AC (1981) The theoretical proportion of the donor genome in near-isogenic lines of self-fertilizers bred by backcrossing. Euphytica 30:227–238. https://doi.org/10.1007/BF00033982
Subedi M, Bazghaleh N, Caudillo-Ruiz K, Vandenberg A (2021) Stemphylium blight reduces milling qualities of lentil. Agron J 113:1909–1919. https://doi.org/10.1002/agj2.20551
Tanksley SD, Hewitt J (1988) Use of molecular markers in breeding for soluble solids content in tomato - a re-examination. Theor Appl Genet 75:811–823. https://doi.org/10.1007/BF00265610
Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277:1063–1066. https://doi.org/10.1126/science.277.5329.1063
Tanksley SD, Nelson JC (1996) Advanced backcross QTL analysis: a method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines. Theor Appl Genet 92:191–203. https://doi.org/10.1007/BF00223376
Tanksley SD, Rick CM (1980) Isozymic gene linkage map of the tomato: applications in genetics and breeding. Theor Appl Genet 58:161–170. https://doi.org/10.1007/BF00279708
Taylor P, Lindbeck K, Chen W, Ford R (2007) Lentil diseases. In: Yadav SS, McNeil DL, Stevenson PC (eds) Lentil: an ancient crop for modern times. Springer, Berlin
Thomma BPHJ, Nürnberger T, Joosten MHAJ (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15. https://doi.org/10.1105/tpc.110.082602
Tullu A, Banniza S, Tar’an B, Warkentin T, Vandenberg A (2010) Sources of resistance to ascochyta blight in wild species of lentil (Lens culinaris Medik.). Genet Resour Crop Evol 57:1053–1063. https://doi.org/10.1007/s10722-010-9547-7
Tullu A, Bett K, Banniza S, Vail S, Vandenberg A (2013) Widening the genetic base of cultivated lentil through hybridization of Lens culinaris “Eston” and L. ervoides accession IG 72815. Can J Plant Sci 93:1037–1047. https://doi.org/10.4141/CJPS2013-072
Vandenberg A, Kiehn FA, Vera C, Gaudiel R, Buchwaldt L, Dueck S et al (2002) CDC Glamis lentil. Can J Plant Sci 82:103–104. https://doi.org/10.4141/P01-001
Vandenberg A, Banniza S, Warkentin TD, Ife S, Barlow B, McHale S et al (2006) CDC redberry lentil. Can J Plant Sci 86:497–498. https://doi.org/10.4141/P05-071
VanRaden PM (2008) Efficient methods to compute genomic predictions. J Dairy Sci 91:4414–4423. https://doi.org/10.3168/jds.2007-0980
Von Korff M, Wang H, Léon J, Pillen K (2005) AB-QTL analysis in spring barley. I. Detection of resistance genes against powdery mildew, leaf rust and scald introgressed from wild barley. Theor Appl Genet 111:583–590. https://doi.org/10.1007/s00122-005-2049-x
Wang J, Zhang Z (2021) GAPIT Version 3: boosting power and accuracy for genomic association and prediction. Genomics Proteomics Bioinf 19:629–640. https://doi.org/10.1016/j.gpb.2021.08.005
Warschefsky E, Penmetsa RV, Cook DR, von Wettberg EJB (2014) Back to the wilds: tapping evolutionary adaptations for resilient crops through systematic hybridization with crop wild relatives. Am J Bot 101:1791–1800. https://doi.org/10.3732/ajb.1400116
Wong MML, Gujaria-Verma N, Ramsay L, Yuan HY, Caron C, Diapari M et al (2015) Classification and characterization of species within the genus lens using genotyping-by-sequencing (GBS). PLoS ONE 10:1–16. https://doi.org/10.1371/journal.pone.0122025
Wu Y, Zhou Z, Dong C, Chen J, Ding J, Zhang X et al (2020) Linkage mapping and genome-wide association study reveals conservative QTL and candidate genes for Fusarium rot resistance in maize. BMC Genomics 21:1–11. https://doi.org/10.1186/s12864-020-6733-7
Yu J (2005) Advanced backcross QTL analysis and genetic study of an introgressed powdery-mildew resistance gene derived from Avena macrostachya in oat (Avena sativa). PhD Dissertation, Martin-Luther-Universität
Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20. https://doi.org/10.3835/plantgenome2008.02.0089
Zohary D (1989) Pulse domestication and cereal domestication: How different are they? Econ Bot 43:31–34. https://doi.org/10.1007/BF02859322
Acknowledgements
Special thank you to Brent Barlow and Kevin Mikituk for technical assistance in the field. We appreciate the Pulse Crop Genetics and Breeding lab members Akiko Tomita and Robert Stonehouse for their assistance with exome capture library preparation for sequencing. We thank Larrisa Ramsay and Carolyn Caron for assistance on bioinformatics. We are also grateful for genetic resources made available from the ‘Application of Genomics to Innovation in Lentil Economy (AGILE)’ project. We acknowledged funding from the Saskatchewan Pulse Growers and the Agricultural Development Fund of the Saskatchewan Ministry of Agriculture.
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Saskatchewan Pulse Growers and the Agricultural Development Fund of the Saskatchewan Ministry of Agriculture.
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All authors contributed to the study design. SA and TSG performed the experiments and data collection. SA analyzed the data and wrote the first draft of the manuscript. SB, TSG, AV advised on the materials and methods, results and discussions. All authors reviewed and approved the final manuscript.
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Adobor, S., Gela, T.S., Banniza, S. et al. Mapping of genomic regions linked to stemphylium blight (Stemphylium botryosum Wallr.) resistance in lentil using linkage mapping and marker-trait association analysis. Euphytica 219, 86 (2023). https://doi.org/10.1007/s10681-023-03215-z
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DOI: https://doi.org/10.1007/s10681-023-03215-z