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Genetic diversity and population structure of rice (Oryza sativa L.) landraces from Kerala, India analyzed through genotyping-by-sequencing

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Abstract

Researchers stand at the vanguard of advancement and application of next-generation sequencing technology for developing dominant strategies for the sustainable management of genetically diverse crops. We attempt to fill the existing research lacuna in the molecular characterization of potent rice landraces in Kerala. Genotyping-by-sequencing (GBS) was performed on 96 Kerala rice accessions to identify single-nucleotide polymorphisms (SNPs), to examine the genetic diversity, population structure, and to delineate linkage disequilibrium (LD) pattern. GBS identified 5856 high-quality SNPs. The structure analysis indicated three subpopulations with the highest probability for population clustering with significant genetic differentiation, confirmed by principal component analysis. The genome-wide LD decay distance was 772 kb, at which the r2 dropped to half its maximum value. The analysis of genetic properties of the identified SNP panel with an average polymorphism information content (PIC) value of 0.22 and a minor allele frequency (MAF) > 0.1 unveiled their efficacy in genome-wide association studies (GWAS). High FST (0.266) and low Nm (0.692) portray a strong genetic differentiation among the rice landraces, complementing the genetic structuring observed in the studied population. Slow LD decay in the rice landraces reflects their self-pollinating behavior and the indirect selection of desired traits by domestication. Moreover, the high LD entails only a minimum number of SNP markers for detecting marker–trait association. The diverse germplasm utilized in this study can be further utilized to disclose genetic variants associated with phenotypic traits and define signatures of selection via GWAS and selective sweep, respectively.

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References

  • Aiswariya K, Thomas G (2016) Characterization of five rice varieties using morphological traits and seed storage protein profiling. South Indian J Biol Sci 2(1):152–161

    Article  Google Scholar 

  • Alipour H, Bihamta MR, Mohammadi V, Peyghambari SA, Bai G, Zhang G (2017) Genotyping-by-sequencing (GBS) revealed molecular genetic diversity of Iranian wheat landraces and cultivars. Front Plant Sci 8:1293

    Article  PubMed  PubMed Central  Google Scholar 

  • Ashraf AM, Lokanadan S (2017) A review of rice landraces in India and its inherent medicinal values-the nutritive food values for future. Int J Curr Microbiol Appl Sci 6(12):348–354

    Article  Google Scholar 

  • Bashir T, Sailer C, Gerber F, Loganathan N, Bhoopalan H, Eichenberger C, Grossniklaus U, Baskar R (2014) Hybridization alters spontaneous mutation rates in a parent-of-origin-dependent fashion in Arabidopsis. Plant Physiol 165(1):424–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Begum H, Spindel JE, Lalusin A, Borromeo T, Gregorio G, Hernandez J, Virk P, Collard B, McCouch SR (2015) Genome-wide association mapping for yield and other agronomic traits in an elite breeding population of tropical rice (Oryza sativa). PLoS ONE 10(3):e0119873

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhandari HR, Bhanu AN, Srivastava K, Singh MN, Shreya HA (2017) Assessment of genetic diversity in crop plants-an overview. Adv Plants Agric Res 7(3):00255

    Google Scholar 

  • Bhuvaneswari S, Krishnan SG, Bollinedi H, Saha S, Ellur RK, Vinod KK, Singh IM, Prakash N, Bhowmick PK, Nagarajan M (2020) Genetic architecture and anthocyanin profiling of aromatic rice from Manipur reveals divergence of Chakhao landraces. Front Genet 11:1166

    Article  Google Scholar 

  • Blakeney M, Krishnankutty J, Raju RK, Siddique KH (2020) Agricultural innovation and the protection of traditional rice varieties: Kerala a case study. Front Sustain Food Syst 3:116

    Article  Google Scholar 

  • Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32(3):314–331

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Cheng J, Kao H, Dong S (2020) Population genetic structure and gene flow of rare and endangered Tetraena mongolica Maxim. revealed by reduced representation sequencing. BMC Plant Biol 20(1):391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crowell S, Korniliev P, Falcao A, Ismail A, Gregorio G, Mezey J, McCouch S (2016) Genome-wide association and high-resolution phenotyping link Oryza sativa panicle traits to numerous trait-specific QTL clusters. Nat Commun 7(1):1–14

    Article  Google Scholar 

  • Descalsota GIL, Swamy BP, Zaw H, Inabangan-Asilo MA, Amparado A, Mauleon R, Chadha-Mohanty P, Arocena EC, Raghavan C, Leung H, Hernandez JE, Lalusin AB, Mendioro MS, Diaz MGQ, Reinke R (2018) Genome-wide association mapping in a rice MAGIC plus population detects QTLs and genes useful for biofortification. Front Plant Sci 9:1347

    Article  PubMed  PubMed Central  Google Scholar 

  • Devi PI, Solomon SS, Narayanan M (2017) Conservation of traditional rice varieties for crop diversity in Kerala. J Res ANGRAU 45:93–99

    Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Earl DA, Vonholdt BM (2012) Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Eltaher S, Sallam A, Belamkar V, Emara HA, Nower AA, Salem KFM, Poland J, Baenziger PS (2018) Genetic diversity and population structure of F3: 6 Nebraska winter wheat genotypes using genotyping-by-sequencing. Front Genet 9:76

    Article  PubMed  PubMed Central  Google Scholar 

  • Feng Y, Lu Q, Zhai R, Zhang M, Xu Q, Yang Y, Wang S, Yuan X, Yu H, Wang Y (2016) Genome wide association mapping for grain shape traits in indica rice. Planta 244(4):819–830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gimhavanekar VJ, Burondkar MM, Bhave SG, Dalvi VV, Thorat BS, Chavan SS, Mahadik SG, Shinde AK (2020) Evaluation of aromatic and non-aromatic rice (Oryza sativa L.) genotypes for physio-chemical, cooking and nutritive quality traits in Konkan region. IJCS 8(5):1410–1416

    CAS  Google Scholar 

  • Girma G, Nida H, Seyoum A, Mekonen M, Nega A, Lule D, Dessalegn K, Bekele A, Gebreyohannes A, Adeyanju A, Tirfessa A, Ayana G, Taddese T, Mekbib F, Belete K, Tesso T, Ejeta G, Mengiste T (2019) A large-scale genome-wide association analyses of Ethiopian sorghum landrace collection reveal loci associated with important traits. Front Plant Sci 10:691

    Article  PubMed  PubMed Central  Google Scholar 

  • Gopi G, Manjula M (2018) Speciality rice biodiversity of Kerala: need for incentivising conservation in the era of changing climate. Curr Sci 114(5):997–1006

    Article  Google Scholar 

  • Govindaraj M, Vetriventhan M, Srinivasan M (2015) Importance of genetic diversity assessment in crop plants and its recent advances: an overview of its analytical perspectives. Genet Res Int 2015:431487

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hill WG, Weir BS (1988) Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol 33(1):54–78

    Article  CAS  PubMed  Google Scholar 

  • Hoang GT, Van Dinh L, Nguyen TT, Ta NK, Gathignol F, Mai CD, Jouannic S, Tran KD, Khuat TH, Do VN, Lebrun M (2019) Genome-wide association study of a panel of Vietnamese rice landraces reveals new QTLs for tolerance to water deficit during the vegetative phase. Rice 12(1):1–20

    Article  Google Scholar 

  • Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang L, Deng L, Li W, Lu Y, Weng Q, Liu K, Huang T, Zhou T, Jing Y, Li W, Lin Z, Buckler ES, Qian Q, Zhang QF, Li J, Han B (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967

    Article  CAS  PubMed  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) Clumpp: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23(14):1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Joseph J, Francies RM, Zachariah G, Av SK (2007) Characterisation of navara (Oryza sativa L.) a traditional medicinal rice of Kerala for qualitative traits. Indian J Agric Res 41(4):267–271

    Google Scholar 

  • Karunakaran N (2014) Paddy cultivation in Kerala-trends, determinants and effects on food security. Artha J Soc Sci 13(4):21–35

    Google Scholar 

  • Kumar PS, Elsy CR, Nazeem PA, Augustin A (2010) Use of different marker systems to estimate genetic diversity in the traditional medicinal rice cultivar of Kerala. Int J Plant Breed Genet 4(2):89–103

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar A, Sharma D, Tiwari A, Jaiswal JP, Singh NK, Sood S (2016) Genotyping-by-sequencing analysis for determining population structure of finger millet germplasm of diverse origins. Plant Genome 9(2):1–15

  • Latha M, Abraham Z, Nair RA, Mani S, Dutta M (2013) Rice landraces of Kerala state of India: a documentation. Int J Biodivers Conserv 5(4):250–263

    Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo Z, Brock J, Dyer JM, Kutchan T, Schachtman D, Augustin M, Ge Y, Fahlgren N, Abdel-Haleem H (2019) Genetic diversity and population structure of a Camelina sativa spring panel. Front Plant Sci 10:184

    Article  PubMed  PubMed Central  Google Scholar 

  • Manickavelu A, Joukhadar R, Jighly A, Lan C, Huerta-Espino J, Stanikzai AS, Kilian A, Singh RP, Ban T (2016) Genome-wide association mapping of stripe rust resistance in Afghan wheat landraces. Plant Sci 252:222–229

    Article  CAS  PubMed  Google Scholar 

  • Manickavelu A, Jighly A, Ban T (2014) Molecular evaluation of orphan Afghan common wheat (Triticum aestivum L.) landraces collected by Dr. Kihara using single nucleotide polymorphic markers. BMC Plant Biol 14:320

    Article  PubMed  PubMed Central  Google Scholar 

  • Manilal KS (1990) Ethnobotany of the rices of Malabar. Contribution to Indian Ethnobotany. Scientific Publishers, pp 243–253

    Google Scholar 

  • Manjunatha GA, Elsy CR, Rajendran P, Joseph J, Francies RM, Krishnan S (2018) DUS characterization of rice (Oryza sativa L.) landraces of Wayanad, Kerala. Electron J Plant Breed 9(2):617–630

    Article  Google Scholar 

  • Mather KA, Caicedo AL, Polato NR, Olsen KM, McCouch S, Purugganan MD (2007) The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics 177(4):2223–2232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mgonja EM, Park CH, Kang H, Balimponya EG, Opiyo S, Bellizzi M, Mutiga SK, Rotich F, Ganeshan VD, Mabagala R, Sneller C, Correll J, Zhou B, Talbot NJ, Mitchell TK, Wang GL (2017) Genotyping-by-sequencing-based genetic analysis of African rice cultivars and association mapping of blast resistance genes against Magnaporthe oryzae populations in Africa. Phytopathology 107(9):1039–1046

    Article  CAS  PubMed  Google Scholar 

  • Mohammadi SA, Prasanna BM (2003) Analysis of genetic diversity in crop plants—salient statistical tools and considerations. Crop Sci 43(4):1235–1248

    Article  Google Scholar 

  • Nimmakayala P, Levi A, Abburi L, Abburi VL, Tomason YR, Saminathan T, Vajja VG, Malkaram S, Reddy R, Wehner TC, Mitchell SE, Reddy UK (2014) Single nucleotide polymorphisms generated by genotyping by sequencing to characterize genome-wide diversity, linkage disequilibrium, and selective sweeps in cultivated watermelon. BMC Genom 15(1):767

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28(19):2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poland JA, Rife TW (2012) Genotyping‐by‐sequencing for plant breeding and genetics. Plant Genome 5:92–102

  • Pradheep K, John KJ, Latha M, Suma A (2021) Status of crop plants of agricultural importance in Kerala state, India: an update. Genet Resour Crop Evol 68:1849–1873

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raj RD, Kiran AG, Thomas G (2010) Population genetic structure and conservation priorities of Oryza rufipogon Griff. populations in Kerala, India. Curr Sci 98(1):65–68

    CAS  Google Scholar 

  • Rajani J, Deepu V, Nair GM, Nair AJ (2013) Molecular characterization of selected cultivars of rice, Oryza sativa L. using random amplified polymorphic DNA (RAPD) markers. Int Food Res J 20(2):919–923

    CAS  Google Scholar 

  • Rao VR, Hodgkin T (2002) Genetic diversity and conservation and utilization of plant genetic resources. Plant Cell Tissue Organ Cult 68(1):1–19

    Article  Google Scholar 

  • Rao IS, Neeraja CN, Srikanth B, Subrahmanyam D, Swamy KN, Rajesh K, Vijayalakshmi P, Kiran TV, Sailaja N, Revathi P, Rao PR (2018) Identification of rice landraces with promising yield and the associated genomic regions under low nitrogen. Sci Rep 8(1):1–13

    Article  Google Scholar 

  • Rathinasabapathi P, Purushothaman N, Ramprasad VL, Parani M (2015) Whole genome sequencing and analysis of Swarna, a widely cultivated indica rice variety with low glycemic index. Sci Rep 5(1):1–10

    Article  Google Scholar 

  • Rekha T, Martin KP, Sreekumar VB, Madassery J (2011) Genetic diversity assessment of rarely cultivated traditional indica rice (Oryza sativa L.) varieties. Biotechnol Res Int. https://doi.org/10.4061/2011/784719

  • Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci 98(20):11479–11484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma SK, MacKenzie K, McLean K, Dale F, Daniels S, Bryan GJ (2018) Linkage disequilibrium and evaluation of genome-wide association mapping models in tetraploid potato. G3 Genes Genomes Genet 8(10):3185–3202

    CAS  Google Scholar 

  • Skaria R, Sen S, Muneer PMA (2011) Analysis of genetic variability in rice varieties (Oryza sativa L.) of Kerala using RAPD markers. J Genet Eng Biotechnol 24:1–9

  • Slatkin M (1985) Gene flow in natural populations. Ann Rev Ecol Syst 16:393–430

    Article  Google Scholar 

  • Soorni A, Fatahi R, Haak DC, Salami SA, Bombarely A (2017) Assessment of genetic diversity and population structure in Iranian cannabis germplasm. Sci Rep 7(1):1–10

    Article  CAS  Google Scholar 

  • Sreejayan KVR, Thomas G (2003) Collecting and morphological evaluation of ‘Njavara’, traditional medicinal rice (Oryza sativa L.) in Kerala. Plant Genet Resour Newsl 135:12–17

  • Sreejayan KUS, Varghese G, Jacob TM, Thomas G (2011) Stratification and population structure of the genetic resources of ancient medicinal rice (Oryza sativa L.) landrace Njavara. Genet Resour Crop Evol 58:697–711

    Article  Google Scholar 

  • Taranto F, D’Agostino N, Greco B, Cardi T, Tripodi P (2016) Genome-wide SNP discovery and population structure analysis in pepper (Capsicum annuum) using genotyping by sequencing. BMC Genom 17(1):943

    Article  CAS  Google Scholar 

  • Thomas J, Dominic VJ (2016) Assessment of genetic diversity and relationship of coastal salt tolerant rice accessions of Kerala (South India) using microsatellite markers. J Plant Mol Breed 4(1):35–42

    Google Scholar 

  • Thomas G, Joseph L, Varghese G (2001) Discrimination between Oryza malampuzhaensis Krish. et Chand. and Oryza officinalis Wall ex Watt based on RAPD markers and morphological traits. Euphytica 122:181–189

    Article  CAS  Google Scholar 

  • Umadevi M, Shanthi P, Saraswathi R (2019) Characterization of rice landraces of Tamil Nadu by multivariate analysis. Electron J Plant Breed 10(3):1185–1193

    Article  Google Scholar 

  • Vanaja T, Randhawa GJ, Mammootty KP (2007) Pedigree evaluation and molecular diversity of some true breeding rice (Oryza sativa L.) genotypes of Kerala. J Trop Agric 44:42–47

    Google Scholar 

  • Vanaja T, Singh R, Randhawa GJ (2010) Genetic relationships among a collection of Indica rice (Oryza sativa) genotypes of Kerala revealed by SSR markers. Indian J Agric Sci 80(3):191

    CAS  Google Scholar 

  • Vasumathy SK, Peringottillam M, Sundaram KT, Kumar SHK, Alagu M (2020) Genome-wide structural and functional variant discovery of rice landraces using genotyping by sequencing. Mol Biol Rep 47:7391–7402

    Article  CAS  PubMed  Google Scholar 

  • Vos PG, Paulo MJ, Voorrips RE, Visser RG, van Eck HJ, van Eeuwijk FA (2017) Evaluation of LD decay and various LD-decay estimators in simulated and SNP-array data of tetraploid potato. Theor Appl Genet 130(1):123–135

    Article  PubMed  Google Scholar 

  • Yang X, Tan B, Liu H, Zhu W, Xu L, Wang Y, Fan X, Sha L, Zhang H, Zeng J, Wu D, Jiang Y, Hu X, Chen G, Zhou Y, Kang H (2020) Genetic diversity and population structure of asian and european common wheat accessions based on genotyping-by-sequencing. Front Genet 11:1157

    Article  Google Scholar 

  • Zhao K, Tung CW, Eizenga GC, Wright MH, Ali ML, Price AH, Norton GJ, Islam MR, Reynolds A, Mezey J, McClung AM (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2(1):1–10

    Article  Google Scholar 

  • Zoríc M, Dodig D, Kobiljski B, Quarrie S, Barnes J (2012) Population structure in a wheat core collection and genomic loci associated with yield under contrasting environments. Genetica 140(4–6):259–275

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge the Central University of Kerala for providing the research facilities. MP extends thanks to the University Grant Commission (UGC) for awarding financial aid.

Funding

This research was supported by grants from the Department of Science and Technology-Science and Engineering Research Board (DST-SERB), Government of India (Grant No. ECR/2016/001934) to AM.

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AM conceived and supervised the research work, and acquired research grant for the research; MP, SKV prepared genetic materials; HKKS, MP performed data analyses; MP wrote the manuscript; all authors read and approved the final manuscript.

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Correspondence to Manickavelu Alagu.

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Peringottillam, M., Kunhiraman Vasumathy, S., Selvakumar, H.K. et al. Genetic diversity and population structure of rice (Oryza sativa L.) landraces from Kerala, India analyzed through genotyping-by-sequencing. Mol Genet Genomics 297, 169–182 (2022). https://doi.org/10.1007/s00438-021-01844-4

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