Skip to main content

Association of functional markers with flowering time in lentil

Journal of Applied Genetics volume 59, pages 9–21 (2018)Cite this article

Abstract

In the present study, a diverse panel of 96 accessions of lentil germplasm was used to study flowering time over environments and to identify simple sequence repeat markers associated with flowering time through association mapping. The study showed high broad sense heritability estimate (h 2 bs=0.93) for flowering time in lentil. Screening of 534 SSR markers resulted in an identification of 75 SSR polymorphic markers (13.9%) across studied genotypes. These markers amplified 266 loci and generated 697 alleles ranging from two to 16 alleles per locus. Model-based cluster analysis used for the determination of population structure resulted in the identification of two distinct subpopulations. Distribution of flowering time was ranged from 40 to 70 days in subpopulation I and from 54 to 69 days in subpopulation II and did not skew either late or early flowering time within a subpopulation. No admixture was observed within the subpopulations. Use of the most accepted maximum likelihood model (P3D mixed linear model with optimum compression) of MTA analysis showed significant association of 26 SSR markers with flowering time at <0.05 probability. The percent of phenotypic explained by each associated marker with flowering time ranged from 2.1 to 21.8% and identified QTLs for flowering time explaining high phenotypic variation across the environments (10.7-21.8%) or in a particular environment (10.2-21.4%). In the present study, 13 EST-SSR showed significant association with flowering time and explained large phenotypic variation (2.3-21.8%) compared to genomic SSR markers (2.1-10.2%). Hence, these markers can be used as functional markers in the lentil breeding program to develop short duration cultivars.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1

References

  • Abdelnoor RV, Barros EG, Moreira (1995) Determination of genetic diversity within Brazilian soybean germplasm using random amplified polymorphic DNA techniques and comparative analysis with pedigree data. Braz J Genet 18:265–273

    CAS  Google Scholar 

  • Anbessa Y, Warkentin T, Vandenberg A, Ball R (2006) Inheritance of time to flowering in chickpea in a short-season temperate environments. J Hered 97:55–61

    CAS  Article  PubMed  Google Scholar 

  • Asghar MJ, Abbas G, Shah TM (2010) Study of genetic diversity in some local and exotic lentil (Lens culinaris Medik) genotypes. Pak J Bot 42:2681–2690

    Google Scholar 

  • Bajaj D, Srivastava R, Nath M, Tripathi S, Bharadwaj C, Upadhyaya HD, Tyagi AK, Parida SK (2016) Ecotilling-based association mapping efficiently delineates functionally relevant natural allelic variants of candidate genes governing agronomic traits in chickpea. Front Plant Sci 2016:7. https://doi.org/10.3389/fpls.2016.00450

    Google Scholar 

  • Basheer-Salimia R, Camilli B, Scacchi S, Noli E, Awad M (2015) Assessment of genetic diversity in lentils (Lens culinaris Medik.) based on SNPs. Genet Mol Res 14:5870–5878

    CAS  Article  PubMed  Google Scholar 

  • Benbouza H, Jacquemin JM, Baudoin JP, Mergeai G (2006) Optimization of a reliable, fast, cheap and sensitive silver staining method to detect SSR markers in polyacrylamide gels. Biotechnol Agron Soc Environ 10(2):77–81

    CAS  Google Scholar 

  • Bradbury P, Parker T, Hamblin MT, Jannink JL (2011) Assessment of power and false discovery rate in genome-wide association studies using the barley CAP germplasm. Crop Sci 51:52–59

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Cheng P, Holdsworth W, Ma Y, Coyne CJ, Mazourek M, Grusak MA, Fuchs S, McGee RJ (2015) Association mapping of agronomic and quality traits in USDA pea single-plant collection. Mol Breed 35(2):75

    Article  Google Scholar 

  • Choudhary AK, Kumar J, Gupta S, Sultana R, Singh IS (2016) Breeding for adaptive traits in pulses. In: Singh (ed) Souvenir & Abstract of National Conference on Bringing Self-sufficiency in Pulses for eastern India. 5–6 August 2016. Bihar Agricultural University, Sabour, pp 36–43

  • Contreras Soto RI, de Oliveira MB, Costenaro da Silva D, Scapim CA, Schuster I (2017) Population structure, genetic relatedness and linkage disequilibrium blocks in cultivars of tropical soybean (Glycine max). Euphytica 213(8):173

    Article  Google Scholar 

  • Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna URL http://www.R-project.org/

    Google Scholar 

  • Dikshit HK, Singh A, Singh D, Aski MS, Prakash P, Jain N, Meena S, Kumar S, Sarker A (2015) Genetic diversity in Lens species revealed by EST and genomic simple sequence repeat analysis. PLOS One 10:e0138101

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Emami MK (1996) Genetic mapping in lentil (Lens culinaris Medik). Ph.D. Thesis. Division of Genetics, Indian Agricultural Research Institute, New Delhi, India

  • Erskine W, Ellis RH, Summerfield RJ, Roberts EH, Hussain A (1990) Characterization of responses to temperature and photoperiod for time to flowering in a world lentil collection. Theor Appl Genet 80(2):193–199

    CAS  Article  PubMed  Google Scholar 

  • Erskine W, Chandra S, Chaudhary M, Malik IA, Sarker A, Sharma B, Tufail M, Tyagi MC (1998) A bottleneck in lentil: widening its genetic base in South Asia. Euphytica 101:207–211

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    CAS  Article  PubMed  Google Scholar 

  • Fratini R, Duran Y, Garcia P, Perez de la Vega M (2007) Identification of quantitative trait loci (QTL) for plant structure, growth habit and yield in lentil. Span J Agric Res 5:348–356

    Article  Google Scholar 

  • Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57:461–485

    CAS  Article  PubMed  Google Scholar 

  • Imaizumi T (2010) Arabidopsis circadian clock and photoperiodism: time to think about location. Curr Opin Plant Biol 13:83–89

    CAS  Article  PubMed  Google Scholar 

  • Ito T, Gyung Tae K, Kazuo S (2000) Disruption of an Arabidopsis cytoplasmic ribosomal protein S13-homologous gene by transposon-mediated mutagenesis causes aberrant growth and development. Plant J 22:257–264

    CAS  Article  PubMed  Google Scholar 

  • Jain N, Dikshit HK, Singh D, Singh A, Kumar H (2013) Discovery of EST-derived microsatellite primers in the legume Lens culinaris (Fabaceae). Appl Pl Sci 1:1200539. https://doi.org/10.3732/apps.1200539

    Article  Google Scholar 

  • Jaiswal V, Mir RR, Mohan A, Balyan HS, Gupta PK (2012) Association mapping for pre-harvest sprouting tolerance in common wheat (Triticum aestivum L.) Euphytica 188:89–102

    CAS  Article  Google Scholar 

  • Jung C, Muller AE (2009) Flowering time control and applications in plant breeding. Trends in Plant Science 14:563–573

    CAS  Article  PubMed  Google Scholar 

  • Kahriman A, Temel HY, Aydoğan A, Tanyolaç MB (2014) Major quantitative trait loci for flowering time in lentil. Turkish J Agric Fores 38:1–8

    Article  Google Scholar 

  • Kandasamy MK, McKinney EC, Meagher RB (2002) Functional non equivalency of actin isovariants in Arabidopsis. Mol Biol Cell 13:251–261

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Kaur S, Cogan NO, Pembleton LW, Shinozuka M, Savin KW, Materne M, Forster JW (2011) Transcriptome sequencing of lentil based on second-generation technology permits large-scale unigene assembly and SSR marker discovery. BMC Genomics 12(1):1

    Article  Google Scholar 

  • Khazaei H, Caron CT, Fedoruk M, Diapari M, Vandenberg A, Coyne CJ, McGee R, Bett KE (2016) Genetic diversity of cultivated lentil (Lens culinaris Medik) and its relation to the world’s agro-ecological zones. Front Plant Sci 7:1093

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar J, Solanki RK (2014) Evaluation of germplasm accessions for agro-morphological traits in lentil. J Food Leg 27:275–280

    Google Scholar 

  • Kumar J, Srivastava E (2014) Impact of reproductive duration on yield and its component traits in lentil. Leg Res 38(2):139–148

    Article  Google Scholar 

  • Kumar J, van Rheenen HA (2000) A major gene for time of flowering in chickpea. J Hered 91:67–68

    CAS  Article  PubMed  Google Scholar 

  • Kumar J, Srivastva E, Singh M, Kumar S, Nadarajan N, Sarker A (2014) Diversification of indigenous gene-pool by using exotic germplasm in lentil (Lens culinaris Medikus subsp. culinaris). Physiol Mol Biol Plants 20(1):125–132

    CAS  Article  PubMed  Google Scholar 

  • Kumar J, Gupta DS, Gupta S, Dubey S, Gupta P, Kumar S (2017) Quantitative trait loci from identification to exploitation for crop improvement. Plant Cell Rep 21:1–27

    CAS  Article  Google Scholar 

  • Kumar S, Rajendran K, Kumar J, Hamwieh A, Baum M (2015) Current knowledge in lentil genomics and its application for crop improvement. Front Plant Sci 6:78

    PubMed  PubMed Central  Google Scholar 

  • Li XJ, Xu X, Yang XM, Li XQ, Liu WH, Gao AN, Li LH (2012) Genetic diversity among a founder parent and widely grown wheat cultivars derived from the same origin based on morphological traits and microsatellite markers. Crop Pasture Sci 63(4):303–310

    CAS  Article  Google Scholar 

  • Lombardi M, Materne M, Cogan NO, Rodda M, Daetwyler HD, Slater AT, Forster JW, Kaur S (2014) Assessment of genetic variation within a global collection of lentil (Lens culinaris Medik.) cultivars and landraces using SNP markers. BMC Genet 15:150

    Article  PubMed  PubMed Central  Google Scholar 

  • Malysheva-Otto LV, Ganal MW, Roder MS (2006) Analysis of molecular diversity, population structure and linkage disequilibrium in a worldwide survey of cultivated barley germplasm (Hordum vulgare L.) BMC Genet 7:6

    Article  PubMed  PubMed Central  Google Scholar 

  • Mandel JR, Nambeesan S, Bowers JE, Marek LF, Ebert D, Rieseberg LH, Knapp SJ, Burke JM (2013) Association mapping and the genomic consequences of selection in sunflower. PLoS Genet 9(3):e1003378. https://doi.org/10.1371/journal.pgen.1003378

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Niu Y, Xu Y, Liu XF, Yang SX, Wei SP, Xie FT, Zhang YM (2013) Association mapping for seed size and shape traits in soybean cultivars. Mol Breed 31(4):785–794

    CAS  Article  Google Scholar 

  • Ostrowski MF, David A, Santoni S, Mckhann H, Reboud X, Corre VL, Camilleri C, Brunel D, Bouchez D, Faure B, Bataillon T (2006) Evidence for a large-scale population structure among accessions of Arabidopsis thaliana: possible causes and consequences for the distribution of linkage disequilibrium. Mol Ecol 15:1507–1517

    CAS  Article  PubMed  Google Scholar 

  • Pasam RK, Sharma R, Malosetti M, van Eeuwijk FA, Haseneyer G, Kilian B, Graner A (2012) Genome-wide association studies for agronomical traits in a worldwide spring barley collection. BMC Plant Biol 12:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000a) Inference of population structure using multi-locus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000b) Association mapping in structured populations. Am J Hum Genet 67:170–181

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Reddy MRK, Rathour R, Kumar N, Katoch P, Sharma TR (2010) Cross-genera legume SSR markers for analysis of genetic diversity in Lens species. Plant Breed 129:514–518

    CAS  Google Scholar 

  • Rosenberg N, Nordborg M (2006) A general population-genetic model for the production by population structure of spurious genotype–phenotype associations in discrete, admixed, or spatially distributed populations. Genetics 173:1665–1678

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Roxrud I, Lid SE, Fletcher JC, Schmidt ED, Opsahl-Sorteberg HG (2007) GASA4, one of the 14-member Arabidopsis GASA family of small polypeptides, regulates flowering and seed development. Plant Cell Physiol 48:471–483

    CAS  Article  PubMed  Google Scholar 

  • Roy JK, Smith KP, Muehlbauer GJ, Chao S, Close TJ, Steffenson BJ (2010) Association mapping of spot blotch resistance in wild barley. Mol Breed 26:243–256

    Article  PubMed  PubMed Central  Google Scholar 

  • Saha GC, Sarker A, Chen W, Vandemark GJ, Muehlbauer FJ (2013) Inheritance and linkage map positions of genes conferring agromorphological traits in Lens culinaris Medik. Intl J Agron. http://dx.doi.org/10.1155/2013/618926

  • Salvi S, Sponza G, Morgante M, Tomes D, Niu X, Fengler KA, Meeley R, Ananiev EV, Svitashev S, Bruggemann E, Li B (2007) Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci 104(27):11376–11381

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Sarker A, Erskine W, Sharma B, Tyagi MC (1999) Inheritance and linkage relationships of days to flower and morphological loci in lentil (Lens culinaris Medikus subsp. culinaris). J Hered 90:270–275

  • Sarker A, Erskine W, Sharma B, Tyagi MC (1999) Inheritance and linkage relationships of days to flower and morphological loci in lentil (Lens culinaris Medikus subsp. culinaris). J Hered 90:270–275

    Article  Google Scholar 

  • Seyedimoradi H, Talebi R (2014) Detecting DNA polymorphism and genetic diversity in lentil (Lens culinaris Medik.) germplasm: comparison of ISSR and DAMD marker. Physiol Mol Biol Plants 20:495–500

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Singh BB, Mishra SK, Sardana S, Dixit GP (2006) Lentil and pea. In: Dhillon BS, Saxena S, Agarwal A, Tyagi RK (eds) Plant genetic resources: food grain crops. Narosa, New Delhi, pp 240–254

  • Singh M, Bisht IS, Kumar S, Dutta M, Bansal KC, Karale M, Sarker A, Amri A, Kumar S, Datta SK (2014) Global wild annual Lens collection: a potential resource for lentil genetic base broadening and yield enhancement. PLoS One 9(9):e107781

    Article  PubMed  PubMed Central  Google Scholar 

  • Šlajcherová K, Fišerová J, Fischer L, Schwarzerová K (2012) Multiple actin isotypes in plants: diverse genes for diverse roles? Front Plant Sci 2012:3

    Google Scholar 

  • Subbarao GV, Kumar Rao JVDK, Kumar J, Johansen C, Deb UK, Ahmed I, Krishna Rao MV, Venkataratnam L, Hebber KR, Sai MVSR, Harris D (2001) Spatial distribution and quantification of rice-fallows in South Asia-potential for legumes. International Crops Research Institute for the Semi-Arid Tropics, Patancheru, p 316

    Google Scholar 

  • Summerfield RJ, Roberts EH (1988) Photo-thermal regulation of flowering in pea, lentil, faba bean and chickpea. In: Summerfield RJ (ed) World crops: cool season food legumes. Current plant science and biotechnology in agriculture, vol 5. Springer, Dordrecht, pp 911–922

  • Summerfield RJ, Muehlbauer FJ, Roberts EH (1985) Lens culinaris. In: Halvey AH (ed) Handbook of flowering, vol 1. CRC, Boca Raton, pp 118–124

  • Sun D, Ren W, Sun G, Peng J (2011) Molecular diversity and association mapping of quantitative traits in Tibetan wild and worldwide originated barley (Hordeum vulgare L.) germplasm. Euphytica 178(1):31–43

    Article  Google Scholar 

  • Szalma SJ, Buckler IVES, Snook ME, McMullen MD (2005) Association analysis of candidate genes for maysin and chlorogenic acid accumulation in maize silks. Theor Appl Genet 110:1324–1333

    CAS  Article  PubMed  Google Scholar 

  • Tahir M, Muehlbauer FJ, Spaeth SC (1994) Association of isozyme markers with quantitative trait loci in random single seed descent derived lines of lentil (Lens culinaris Medik.) Euphytica 75:111–119

    Article  Google Scholar 

  • Takahashi Y, Teshima KM, Yokoi S, Innan H, Shimamoto K (2009) Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proc Natl Acad Sci USA 106:4555–4560

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Thines BC, Youn Y, Duarte MI, Harmon FG (2014) The time of day effects of warm temperature on flowering time involve PIF4 and PIF5. J Exp Bot 65:1141–1151

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Topal A, Aydın C, Akgün N, Babaoglu M (2004) Diallel cross analysis in durum wheat (Triticum durum Desf.): identification of best parents for some kernel physical features. Field Crops Research 87(1):1–2

    Article  Google Scholar 

  • Tullu A, TarTa B, Warkentin T, Vandenberg A (2008) Construction of an intraspecific linkage map and QTL analysis for earliness and plant height in lentil. Crop Sci. 48:2254–2264

    Article  Google Scholar 

  • Verma P, Shah N, Bhatia S (2013) Development of an expressed gene catalogue and molecular markers from the de novo assembly of short sequence reads of the lentil (Lens culinaris Medik.) transcriptome. Plant Biotechnol J 11:894–905

    CAS  Article  PubMed  Google Scholar 

  • Verma P, Sharma TR, Srivastava PS, Abdin MZ, Bhatia S (2014) Exploring genetic variability within lentil (Lens culinaris Medik.) and across related legumes using a newly developed set of microsatellite markers. Mol Biol Rep 41:5607–5625

    CAS  Article  PubMed  Google Scholar 

  • Visioni A, Tondelli A, Francia E, Pswarayi A, Malosetti M, Russell J, Thomas W, Waugh R, Pecchioni N, Romagosa I, Comadran J (2013) Genome-wide association mapping of frost tolerance in barley (Hordeum vulgare L.) BMC Genomics 14:424

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Wang YH, Bible P, Loganantharaj R, Upadhyaya HD (2012) Identification of SSR markers associated with height using pool-based genome-wide association mapping in sorghum. Mol Breed 30:281–292

    Article  Google Scholar 

  • Welch SM, Dong Z, Roe JL, Das S (2005) Flowering time control: gene network modelling and the link to quantitative genetics: modelling complex traits for plant improvement. Aust J Agr Res 56:919–936

    Article  Google Scholar 

  • Wilson LM, Whitt SR, Ibáñez AM, Rocheford TR, Goodman MM, Buckler ES (2004) Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 16:2719–2733

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Yan J, Warburton M, Crouch J (2011) Association mapping enhancing maize (Zea mays L.) genetic improvement. Crop Sci 51:433–449

    Article  Google Scholar 

  • Zhang P, Liu X, Tong H, Lu Y, Li J (2014) Association mapping for important agronomic traits in core collection of rice (Oryza sativa L.) with SSR markers. PloS One 9(10):e111508

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Yang C, Peng J, Sun S, Wang X (2009) GASA5, a regulator of flowering time and stem growth in Arabidopsis thaliana. Plant Mol Biol 69:745–759

    CAS  Article  PubMed  Google Scholar 

  • Zhang S, Cheng F, Wang C, Zhang L, An Y (2013) Cloning and tissue-specific expression of predicted Pisum sativum actin isoform PEAc14-1. Bioch Genet 51:722–727

    CAS  Article  Google Scholar 

  • Zhao Y, Wang H, Chen W, Li Y (2014) Genetic structure, linkage disequilibrium and association mapping of verticillium wilt resistance in elite cotton (Gossypium hirsutum L.) germplasm population. PLoS One 9(1):e86308. https://doi.org/10.1371/journal.pone.0086308

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank the Indian Council of Agricultural Research, New Delhi for research support. This work is partially funded by the Department of Agriculture Corporation and Framers Welfare (DAC & FW), Government of India, New Delhi and Department of Biotechnology (BT/PR10921/AG11/106/943/2014), Govt. of India.

Author information

Affiliations

  1. Division of Crop Improvement, ICAR-Indian Institute of Pulses Research, Kanpur, India

    Jitendra Kumar, Sunanda Gupta, Revanappa S. Biradar, Priyanka Gupta, Sonali Dubey & Narendra Pratap Singh

Authors
  1. Jitendra Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sunanda Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Revanappa S. Biradar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Priyanka Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sonali Dubey
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Narendra Pratap Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JK designed the work, analyzed and interpreted the results, and drafted the manuscript. RSB, SG, SD, and PG helped in collection and tabulation of genotypic and phenotypic data. NPS helped to edit the revised manuscript.

Corresponding author

Correspondence to Jitendra Kumar.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by: Barbara Naganowska

Electronic supplementary material

ESM 1

(DOCX 24 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kumar, J., Gupta, S., Biradar, R.S. et al. Association of functional markers with flowering time in lentil. J Appl Genetics 59, 9–21 (2018). https://doi.org/10.1007/s13353-017-0419-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13353-017-0419-0

Keywords

  • Lentil
  • Flowering time
  • Genetic diversity
  • Population structure
  • Association mapping
  • Functional markers