Abstract
An effort was made in the present study to identify the main effect and epistatic quantitative trait locus (QTL) for the morphological and yield-related traits in peanut. A recombinant inbred line (RIL) population derived from TAG 24 × GPBD 4 was phenotyped in seven environments at two locations. QTL analysis with available genetic map identified 62 main-effect QTLs (M-QTLs) for ten morphological and yield-related traits with the phenotypic variance explained (PVE) of 3.84–15.06%. Six major QTLs (PVE > 10%) were detected for PLHT, PPP, YPP, and SLNG. Stable M-QTLs appearing in at least two environments were detected for PLHT, LLN, YPP, YKGH, and HSW. Five M-QTLs governed two traits each, and 16 genomic regions showed co-localization of two to four M-QTLs. Intriguingly, a major QTL reported to be linked to rust resistance showed pleiotropic effect for yield-attributing traits like YPP (15.06%, PVE) and SLNG (13.40%, PVE). Of the 24 epistatic interactions identified across the traits, five interactions involved six M-QTLs. Three interactions were additive × additive and remaining two involved QTL × environment (QE) interactions. Only one major M-QTL governing PLHT showed epistatic interaction. Overall, this study identified the major M-QTLs for the important productivity traits and also described the lack of epistatic interactions for majority of them so that they can be conveniently employed in peanut breeding.
Similar content being viewed by others
Change history
01 June 2018
The published online version of this article unfortunately missed to capture Rajeev K. Varshney as co-corresponding author. There should have been two corresponding authors for this paper (Rajeev K. Varshney and Ramesh S. Bhat). The correct declaration is shown below.
References
Bertioli DJ, Cannon SB, Froenicke L, Huang G, Farmer AD, Cannon EK, Liu X, Gao D, Clevenger J, Dash S, Ren L, Moretzsohn MC, Shirasawa K, Huang W, Vidigal B, Abernathy B, Chu Y, Niederhuth CE, Umale P, Araujo AC, Kozik A, Do Kim K, Burow MD, Varshney RK, Wang X, Zhang X, Barkley N, Guimaraes PM, Isobe S, Guo B, Liao B, Stalker HT, Schmitz RJ, Scheffler BE, Leal-Bertioli SC, Xun X, Jackson SA, Michelmore R, Ozias-Akins P (2016) The genome sequences of Arachis duranensis and Arachis ipaensis, the diploid ancestors of cultivated peanut. Nat Genet 48(4):438–446. https://doi.org/10.1038/ng.3517
Bocianowski J (2013) Epistasis interaction of QTL effects as a genetic parameter influencing estimation of the genetic additive effect. Genet Mol Biol 36(1):093–100. https://doi.org/10.1590/S1415-47572013000100013
Carlborg Ö, Haley CS (2004) Epistasis: too often neglected in complex trait studies? Nat Rev Genet 5(8):618–625. https://doi.org/10.1038/nrg1407
Chen W, Jiao Y, Cheng L, Huang L, Liao B, Tang M, Ren X, Zhou X, Chen Y, Jiang H (2016a) Quantitative trait locus analysis for pod-and kernel-related traits in the cultivated peanut (Arachis hypogaea L.) BMC Genet 17(1):25. https://doi.org/10.1186/s12863-016-0337-x
Chen X, Li H, Pandey MK, Yang Q, Wang X, Garg V, Chi X, Doddamani D, Hong Y, Upadhyaya H, Guo H, Khan AW, Zhu F, Zhang X, Pan L, Pierce GJ, Zhou G, Krishnamohan KA, Chen M, Zhong N, Agarwal G, Li S, Chitikineni A, Zhang GQ, Sharma S, Chen N, Liu H, Janila P, Wang M, Wang T, Sun J, Li X, Li C, Yu L, Wen S, Singh S, Yang Z, Zhao J, Zhang C, Yu Y, Bi J, Liu ZJ, Paterson AH, Wang S, Liang X, Varshney RK, Yu S (2016b) Draft genome of the peanut A-genome progenitor (Arachis duranensis) provides insights into geocarpy, oil biosynthesis, and allergens. Proc Natl Acad Sci 113(24):6785–6790. https://doi.org/10.1073/pnas.1600899113
Dwivedi S, Thendapani K, Nigam S (1989) Heterosis and combining ability studies and relationship among fruit and seed characters in peanut. Peanut Sci 16(1):14–20. https://doi.org/10.3146/i0095-3679-16-1-4
FAOSTAT (2016) FAO statistical database. http://faostat.fao.org
Gautami B, Pandey MK, Vadez V, Nigam SN, Ratnakumar P, Krishnamurthy L, Radhakrishnan T, Gowda MV, Narasu ML, Hoisington DA, Knapp SJ, Varshney RK (2012) Quantitative trait locus analysis and construction of consensus genetic map for drought tolerance traits based on three recombinant inbred line populations in cultivated groundnut (Arachis hypogaea L.) Mol Breed 30(2):757–772. https://doi.org/10.1007/s11032-011-9660-0
GenStat Committee (2010) Genstat v12.2, VSN International. http://www.vsni.co.uk/downloads/genstat/12th-edition-upgrade
Gowda MVC, Motagi BN, Naidu GK, Diddimani SB, Sheshagiri R (2002) GPBD 4: a spanish bunch groundnut genotype resistant to rust and late leaf spot. Int Arachis News Lett 22:29–32
Hake AA, Shirasawa K, Yadawad A, Sukruth M, Patil M, Nayak SN, Lingaraju S, Patil PV, Nadaf HL, Gowda MVC, Bhat RS (2017) Mapping of important taxonomic and productivity traits using genic and non-genic transposable element markers in peanut (Arachis hypogaea L.) PLoS One 12(10):e0186113. https://doi.org/10.1371/journal.pone.0186113 eCollection 2017
Han S, Liu H, Yan M, Qi F, Wang Y, Sun Z, Huang B, Dong W, Tang F, Zhang X (2017) Differential gene expression in leaf tissues between mutant and wild-type genotypes response to late leaf spot in peanut (Arachis hypogaea L.) PLoS One 12(8):e0183428. https://doi.org/10.1371/journal.pone.0183428
Khedikar Y, Gowda MVC, Sarvamangala C, Patgar K, Upadhyaya HD, Varshney R (2010) A QTL study on late leaf spot and rust revealed one major QTL for molecular breeding for rust resistance in groundnut (Arachis hypogaea L.) Theor Appl Genet 121(5):971–984. https://doi.org/10.1007/s00122-010-1366-x
Kolekar RM, Sujay V, Shirasawa K, Sukruth M, Khedikar YP, Gowda MVC, Pandey MK, Varshney RK, Bhat RS (2016) QTL mapping for late leaf spot and rust resistance using an improved genetic map and extensive phenotypic data on a recombinant inbred line population in peanut (Arachis hypogaea L.) Euphytica 209(1):147–156. https://doi.org/10.1007/s10681-016-1651-0
Kolekar RM, Sukruth M, Nadaf HL, Motagi BN, Lingaraju S, Patil PV, Bhat RS (2017) Marker-assisted backcrossing to develop foliar disease resistant genotypes in TMV 2 variety of peanut (Arachis hypogaea L.). Plant Breed. https://doi.org/10.1111/pbr.12549
Kover PX, Valdar W, Trakalo J, Scarcelli N, Ehrenreich IM, Purugganan MD, Durrant C, Mott R (2009) A multiparent advanced generation inter-cross to fine-map quantitative traits in Arabidopsis thaliana. PLoS Genet 5(7):e1000551. https://doi.org/10.1371/journal.pgen.1000551
Layrisse A, Wynne J, Isleib T (1980) Combining ability for yield, protein and oil of peanut lines from South American centers of diversity. Euphytica 29(3):561–570. https://doi.org/10.1007/BF00023203
Luo H, Ren X, Li Z, Xu Z, Li X, Huang L, Zhou X, Chen Y, Chen W, Lei Y, Liao B, Pandey MK, Varshney RK, Guo B, Jiang X, Liu F, Jiang H (2017a) Co-localization of major quantitative trait loci for pod size and weight to a 3.7 cM interval on chromosome A05 in cultivated peanut (Arachis hypogaea L.) BMC Genomics 18(1):58. https://doi.org/10.1186/s12864-016-3456-x
Luo H, Xu Z, Li Z, Li X, Lv J, Ren X, Huang L, Zhou X, Chen Y, Yu J (2017b) Development of SSR markers and identification of major quantitative trait loci controlling shelling percentage in cultivated peanut (Arachis hypogaea L.). Theor Appl Genet 1–14
Pandey MK, Upadhyaya HD, Rathore A, Vadez V, Sheshshaye MS, Sriswathi M, Govil M, Kumar A, Gowda MVC, Shivali S, Hamidou F, Anil Kumar V, Khera P, Bhat RS, Khan Amir W, Sube S, Hongjie L, Emmanuel M, Nadaf HL, Mukri G, Liang X, Jackson S, Varshney RK (2014a) Genomewide association studies for 50 agronomic traits in peanut using the reference set comprising 300 genotypes from 48 countries of semi-arid tropics of the world. PLoS One 9(8):e105228. https://doi.org/10.1371/journal.pone.0105228
Pandey MK, Wang ML, Qiao L, Feng S, Khera P, Wang H, Tonnis B, Barkley NA, Wang J, Holbrook CC (2014b) Identification of QTLs associated with oil content and mapping FAD2 genes and their relative contribution to oil quality in peanut (Arachis hypogaea L.) BMC Genet 15(1):133. https://doi.org/10.1186/s12863-014-0133-4
Pandey MK, Agarwal G, Kale SM, Clevenger J, Nayak SN, Sriswathi M, Chitikineni A, Chavarro C, Chen X, Upadhyaya HD (2017a) Development and evaluation of a high density genotyping ‘Axiom_Arachis’ array with 58 K SNPs for accelerating genetics and breeding in groundnut. Sci Rep 7:40577. https://doi.org/10.1038/srep40577
Pandey MK, Khan AW, Singh VK, Vishwakarma MK, Shasidhar Y, Kumar V, Garg V, Bhat RS, Chitikineni A, Janila P, Guo B, Varshney RK (2017b) QTL-seq approach identified genomic regions and diagnostic markers for rust and late leaf spot resistance in groundnut (Arachis hypogaea L.) Plant Biotechnol J 15(8):927–941. https://doi.org/10.1111/pbi.12686
Patil S, Kale D, Deshmukh S, Fulzele G, Weginwar B (1995) Semi-dwarf, early maturing and high yielding new groundnut variety, TAG-24. J Oilseeds Res 12:254–257
R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ravi K, Vadez V, Isobe S, Mir RR, Guo Y, Nigam SN, Gowda MVC, Radhakrishnan T, Bertioli DJ, Knapp SJ (2011) Identification of several small main-effect QTLs and a large number of epistatic QTLs for drought tolerance related traits in groundnut (Arachis hypogaea L.) Theor Appl Genet 122(6):1119–1132. https://doi.org/10.1007/s00122-010-1517-0
Sujay V, Gowda MVC, Pandey MK, Bhat RS, Khedikar YP, Nadaf HL, Gautami B, Sarvamangala C, Lingaraju S, Radhakrishan T, Knapp SJ, Varshney RK (2012) QTL analysis and construction of consensus genetic map for foliar disease resistance based on two RIL populations in cultivated groundnut (Arachis hypogaea L.) Mol Breed 30(2):773–788. https://doi.org/10.1007/s11032-011-9661-z
Sukruth M, Paratwagh SA, Sujay V, Varshakumari, Gowda MVC, Nadaf HL, Motagi BN, Lingaraju S, Pandey MK, Varshney RK, Bhat RS (2015) Validation of markers linked to late leaf spot and rust resistance, and selection of superior genotypes among diverse recombinant inbred lines and backcross lines in peanut (Arachis hypogaea L.) Euphytica 204(2):343–351. https://doi.org/10.1007/s10681-014-1339-2
Upadhyaya HD, Nigam S (1998) Epistasis for vegetative and reproductive traits in peanut. Crop Sci 38(1):44–49. https://doi.org/10.2135/cropsci1998.0011183X003800010008x
Varshney RK, Mohan SM, Gaur PM, Gangarao N, Pandey MK, Bohra A, Sawargaonkar SL, Gorantla A, Kimurto PK, Janila P (2013) Achievements and prospects of genomics-assisted breeding in three legume crops of the semi-arid tropics. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2013.1001.1001
Varshney RK, Pandey MK, Pasupuleti J, Nigam SN, Sudini H, Gowda MVC, Sriswathi M, Radhakrishan T, Manohar SS, Patne N (2014) Marker-assisted introgression of a QTL region to improve rust resistance in three elite and popular varieties of peanut (Arachis hypogaea L.) Theor Appl Genet 127(8):1771–1781. https://doi.org/10.1007/s00122-014-2338-3
Vishwakarma MK, Nayak L SN, Guo B, Wan L, Liao B, Varshney RK, Pandey MK (2017) Classical and molecular approaches for mapping of genes and quantitative trait loci in peanut (Arachis hypogaea L.). In: Varshney RK, Pandey MK, Puppala N (eds) The peanut genome. pp 93-116. https://doi.org/10.1007/978-3-319-63935-2
Wang S, Basten C, Zeng Z (2007) Windows QTL cartographer 2.5. North Carolina State University, Raleigh
Wang ML, Khera P, Pandey MK, Wang H, Qiao L, Feng S, Tonnis B, Barkley NA, Pinnow D, Holbrook CC (2015) Genetic mapping of QTLs controlling fatty acids provided insights into the genetic control of fatty acid synthesis pathway in peanut (Arachis hypogaea L.) PLoS One 10(4):e0119454. https://doi.org/10.1371/journal.pone.0119454
Yang J, Hu C, Hu H, Yu R, Xia Z, Ye X, Zhu J (2008) QTLNetwork: mapping and visualizing genetic architecture of complex traits in experimental populations. Bioinformatics 24(5):721–723. https://doi.org/10.1093/bioinformatics/btm494
Yeri SB, Bhat RS (2016) Development of late leaf spot and rust resistant backcross lines in JL 24 variety of groundnut (Arachis hypogaea L.) Electron J Plant Breed 7(1):37–41. https://doi.org/10.5958/0975-928X.2016.00005.3
Yeri SB, Shirasawa K, Pandey MK, Gowda MVC, Sujay V, Shriswathi M, Nadaf HL, Motagi BN, Lingaraju S, Bhat ARS, Varshney RK, Krishnaraj PU, Bhat RS (2014) Development of NILs from heterogeneous inbred families for validating the rust resistance QTLs in peanut (Arachis hypogaea L.) Plant Breed 133(1):80–85. https://doi.org/10.1111/pbr.12130
Yin D, Wang Y, Zhang X, Ma X, He X, Zhang J (2017) Development of chloroplast genome resources for peanut (Arachis hypogaea L.) and other species of Arachis. Sci Rep 7(1):11649. https://doi.org/10.1038/s41598-017-12026-x
Yu SB, Li JX, Xu CG, Tan YF, Gao YJ, Li XH, Zhang Q, Maroof MAS (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci 94(17):9226–9231. https://doi.org/10.1073/pnas.94.17.9226
Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136(4):1457–1468
Zhang X, Zhang J, He X, Wang Y, Ma X, Yin D (2017) Genome-wide association study of major agronomic traits related to domestication in peanut. Front Plant Sci 8:1611. https://doi.org/10.3389/fpls.2017.01611
Zhao C, Qiu J, Agarwal G, Wang J, Ren X, Xia H, Guo B, Ma C, Wan S, Bertioli DJ (2017) Genome-wide discovery of microsatellite markers from diploid progenitor species, Arachis duranensis and A. ipaensis, and their application in cultivated peanut (A. hypogaea). Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.01209
Zhu H, Liu Z, Fu X, Dai Z, Wang S, Zhang G, Zeng R, Liu G (2015) Detection and characterization of epistasis between QTLs on plant height in rice using single segment substitution lines. Breed Sci 65(3):192–200. https://doi.org/10.1270/jsbbs.65.192
Acknowledgements
This work has been undertaken as part of the CGIAR Research Program on Grain Legumes. ICRISAT is a member of CGIAR Consortium. The authors would like to thank Erin Higgins for valuable comments to improve the quality of the manuscript.
Funding
The work presented in this article is a contribution from research projects sponsored by National Funds for Basic Strategic and Frontier Application Research in Agriculture (NFBSFARA) of Indian Council of Agricultural Research (ICAR), New Delhi, India, and World Bank assisted Karnataka Watershed Development Project-II (KWDP-II) funded by Government of Karnataka (GoK), India.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Electronic supplementary material
Supplementary Figure S1
Heatmap of Pearson’s correlation coefficients (r) for all the traits in each environment. The significant correlations are color-coded. (PDF 154 kb)
Supplementary Figure S2
Major effect QTLs detected for agro-morphological traits among the RILs of peanut. (PDF 101 kb)
Supplementary Figure S3
QTL cartographer plot showing co-mapped QTLs for different agro-morphological traits among the RILs of peanut. (PDF 157 kb)
Supplementary Table S1
(XLSX 14 kb)
Supplementary Table S2
(XLSX 17 kb)
Supplementary Table S3
(XLSX 16 kb)
Rights and permissions
About this article
Cite this article
Khedikar, Y., Pandey, M.K., Sujay, V. et al. Identification of main effect and epistatic quantitative trait loci for morphological and yield-related traits in peanut (Arachis hypogaea L.). Mol Breeding 38, 7 (2018). https://doi.org/10.1007/s11032-017-0764-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-017-0764-z