High-density genetic mapping enhances genomic selection accuracy for complex traits in Populus

Abstract

Populus species, important economic species combining rapid growth with broad ecological adaptability, play a critical role in sustainable forestry and bioenergy production. In this study, we performed whole-genome resequencing of 707 individuals from a full-sib family to develop comprehensive single nucleotide polymorphism (SNP) markers and constructed a high-density genetic linkage map of 19 linkage groups. The total genetic length of the map reached 3623.65 cM with an average marker interval of 0.34 cM. By integrating multidimensional phenotypic data, 89 quantitative trait loci (QTL) associated with growth, wood physical and chemical properties, disease resistance, and leaf morphology traits were identified, with logarithm of odds (LOD) scores ranging from 3.13 to 21.72 and phenotypic variance explained between 1.7 and 11.6%. Notably, pleiotropic analysis revealed significant colocalization hotspots on chromosomes LG1, LG5, LG6, LG8, and LG14, with epistatic interaction network analysis confirming genetic basis of coordinated regulation across multiple traits. Functional annotation of 207 candidate genes showed that R2R3-MYB and bHLH transcription factors and pyruvate kinase-encoding genes were significantly enriched, suggesting crucial roles in lignin biosynthesis and carbon metabolic pathways. Allelic effect analysis indicated that the frequency of favorable alleles associated with target traits ranged from 0.20 to 0.55. Incorporation of QTL-derived favorable alleles as random effects into Bayesian-based genomic selection models led to an increase in prediction accuracy ranging from 1 to 21%, with Bayesian ridge regression as the best predictive model. This study provides valuable genomic resources and genetic insights for deciphering complex trait architecture and advancing molecular breeding in poplar.

Keywords

Genomic selection / Genetic map / Quantitative trait loci / Growth / Disease resistance

References

[1] Ahmed AKM, Jiang LP, Wang F, Chen S, Zhou XY, Pei XN, Zhao XY, Qu GZ. Variation analysis of growth traits of four poplar clones under different water and fertilizer management. J for Res, 2020, 31(1): 45-55.

[2] Alemu A, Åstrand J, Montesinos-López OA, Isidro y Sánchez J, Fernández-Gónzalez J, Tadesse W, Vetukuri RR, Carlsson AS, Ceplitis A, Crossa J, Ortiz R, Chawade A. Genomic selection in plant breeding: key factors shaping two decades of progress. Mol Plant, 2024, 17(4): 552-578.

[3] Arends D, Prins P, Jansen RC, Broman KW. R/qtl: high-throughput multiple QTL mapping. Bioinformatics, 2010, 26(23): 2990-2992.

[4] Bradshaw HD, Villar M, Watson BD, Otto KG, Stewart S, Stettler RF. Molecular genetics of growth and development in Populus. III. a genetic linkage map of a hybrid poplar composed of RFLP, STS, and RAPD markers. Theor Appl Genet, 1994, 89(2–3): 167-178.

[5] Broman KW, Wu H, Sen S, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics, 2003, 19(7): 889-890.

[6] Browning BL, Tian XW, Zhou Y, Browning SR. Fast two-stage phasing of large-scale sequence data. Am J Hum Genet, 2021, 108(10): 1880-1890.

[7] Cervera MT, Storme V, Ivens B, Gusmão J, Liu BH, Hostyn V, Van Slycken J, Van Montagu M, Boerjan W. Dense genetic linkage maps of three Populus species (Populus deltoides, P. nigra and P. trichocarpa) based on AFLP and microsatellite markers. Genetics, 2001, 158(2): 787-809.

[8] Chen YN, Wu HT, Dai XG, Li WQ, Qiu Y, Yang YH, Yin TM. Sex effect on growth performance and marker-aided sex discrimination of seedlings of Populus deltoides. J Forestry Res, 2023, 34(5): 1639-1645.

[9] Cui F, Zhang N, Fan XL, Zhang W, Zhao CH, Yang LJ, Pan RQ, Chen M, Han J, Zhao XQ, Ji J, Tong YP, Zhang HX, Jia JZ, Zhao GY, Li JM. Utilization of a Wheat660K SNP array-derived high-density genetic map for high-resolution mapping of a major QTL for kernel number. Sci Rep, 2017, 7(1): 3788.

[10] Du QZ, Gong CR, Wang QS, Zhou DL, Yang HJ, Pan W, Li BL, Zhang DQ. Genetic architecture of growth traits in Populus revealed by integrated quantitative trait locus (QTL) analysis and association studies. New Phytol, 2016, 209(3): 1067-1082.

[11] Fang LC, Liu HL, Wei SY, Keefover-Ring K, Yin TM. High-density genetic map of Populus deltoides constructed by using specific length amplified fragment sequencing. Tree Genet Genomes, 2018, 14(5. 79

[12] Feng L, He YC, Li X, Zhou MQ, Wang C. Analysis of genes related to xylem cell wall development based on transcriptomics in Populus alba ‘Berolinensis’ tension wood. J Forestry Res, 2024, 35(1): 68.

[13] Gaudet M, Jorge V, Paolucci I, Beritognolo I, Mugnozza GS, Sabatti M. Genetic linkage maps of Populus nigra L. including AFLPs, SSRs, SNPs, and sex trait. Tree Genet Genomes, 2008, 4(1): 25-36.

[14] Grattapaglia D, Resende MDV. Genomic selection in forest tree breeding. Tree Genet Genomes, 2011, 7(2): 241-255.

[15] Hayes BJ, Bowman PJ, Chamberlain AJ, Goddard ME. Invited review: Genomic selection in dairy cattle: progress and challenges. J Dairy Sci, 2009, 92(2): 433-443.

[16] Holderegger R, Angelone S, Brodbeck S, Csencsics D, Gugerli F, Hoebee SE, Finkeldey R. Application of genetic markers to the discrimination of European Black Poplar (Populus nigra) from American Black Poplar (P. deltoides) and Hybrid Poplars (P. x canadensis) in Switzerland. Trees, 2005, 19(6): 743-748.

[17] Jackson C, Christie N, Reynolds SM, Marais GC, Tii-kuzu Y, Caballero M, Kampman T, Visser EA, Naidoo S, Kain D, Whetten RW, Isik F, Wegrzyn J, Hodge GR, Acosta JJ, Myburg AA. A genome-wide SNP genotyping resource for tropical pine tree species. Mol Ecol Resour, 2022, 22(2): 695-710.

[18] Jia JZ, Zhao SC, Kong XY, Li YR, Zhao GY, He WM, Appels R, Pfeifer M, Tao Y, Zhang XY, Jing RL, Zhang C, Ma YZ, Gao LF, Gao C, Spannagl M, Mayer KFX, Li D, Pan SK, Zheng FY, Hu Q, Xia XC, Li JW, Liang QS, Chen J, Wicker T, Gou CY, Kuang HH, He GY, Luo YD, Keller B, Xia QJ, Lu P, Wang JY, Zou HF, Zhang RZ, Xu JY, Gao JL, Middleton C, Quan ZW, Liu GM, Wang J, Yang HM, Liu X, He ZH, Mao L, Wang J. Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature, 2013, 496(7443): 91-95.

[19] Liu XT, Zhao QH, Yin P, Li HX, Li XS, Wu LG, Li YJ, Hu YB, Zhao XY. Variation and stability analysis of growth traits of poplar clones in the seedling stage in northeast China. J Forestry Res, 2023, 34(4): 1107-1116.

[20] McLean D, Apiolaza L, Paget M, Klápště J. Simulating deployment of genetic gain in a Radiata pine breeding program with genomic selection. Tree Genet Genomes, 2023, 19(4. 33

[21] Meuwissen TH, Hayes BJ, Goddard ME. Prediction of total genetic value using genome-wide dense marker maps. Genetics, 2001, 157(4): 1819-1829.

[22] Mousavi M, Tong CF, Liu FX, Tao ST, Wu JY, Li HG, Shi JS. De novo SNP discovery and genetic linkage mapping in poplar using restriction site associated DNA and whole-genome sequencing technologies. BMC Genomics, 2016, 17: 656.

[23] Niemczyk M. The effects of cultivar and rotation length (5 vs. 10 years) on biomass production and sustainability of poplar (Populus spp.) bioenergy plantation. GCB Bioenergy, 2021, 13(6): 999-1014.

[24] Ouellette LA, Reid RW, Blanchard SG, Brouwer CR. Linkagemapview—rendering high-resolution linkage and QTL maps. Bioinformatics, 2018, 34(2): 306-307.

[25] Pakull B, Groppe K, Meyer M, Markussen T, Fladung M. Genetic linkage mapping in aspen (Populus tremula L. and Populus tremuloides Michx.). Tree Genet Genomes, 2009, 5(3): 505-515.

[26] Paolucci I, Gaudet M, Jorge V, Beritognolo I, Terzoli S, Kuzminsky E, Muleo R, Scarascia Mugnozza G, Sabatti M. Genetic linkage maps of Populus alba L. and comparative mapping analysis of sex determination across Populus species. Tree Genet Genomes, 2010, 6(6): 863-875.

[27] Pérez P, de los Campos G. Genome-wide regression and prediction with the BGLR statistical package. Genetics, 2014, 198(2): 483-495.

[28] Rafalski JA. Novel genetic mapping tools in plants: SNPs and LD-based approaches. Plant Sci, 2002, 162(3): 329-333.

[29] Rastas P. Lep-MAP3: robust linkage mapping even for low-coverage whole genome sequencing data. Bioinformatics, 2017, 33(23): 3726-3732.

[30] Rastas P, Calboli FCF, Guo BC, Shikano T, Merilä J. Construction of ultradense linkage maps with lep-MAP2: stickleback F₂ recombinant crosses as an example. Genome Biol Evol, 2016, 8(1): 78-93.

[31] Rodríguez del Río Á, Giner-Lamia J, Cantalapiedra CP, Botas J, Deng ZQ, Hernández-Plaza A, Munar-Palmer M, Santamaría-Hernando S, Rodríguez-Herva JJ, Ruscheweyh HJ, Paoli L, Schmidt TSB, Sunagawa S, Bork P, López-Solanilla E, Coelho LP, Huerta-Cepas J. Functional and evolutionary significance of unknown genes from uncultivated taxa. Nature, 2024, 626(7998): 377-384.

[32] Rodríguez-Álvarez MX, Boer MP, van Eeuwijk FA, Eilers PHC. Correcting for spatial heterogeneity in plant breeding experiments with P-splines. Spatial Stat, 2018, 23: 52-71.

[33] Schneider CA, Rasband WS, Eliceiri KW. NIH image to ImageJ: 25 years of image analysis. Nat Methods, 2012, 9(7): 671-675.

[34] Stanton BJ, Neale DB, Li SW (2010) Populus Breeding: from the classical to the genomic approach. In: Genetics and genomics of Populus. Springer, New York, pp 309–348. https://doi.org/10.1007/978-1-4419-1541-2_14

[35] Su JS, Lu ZW, Zeng JW, Zhang XF, Yang XW, Wang SY, Zhang F, Jiang JF, Chen FD. Multi-locus genome-wide association study and genomic prediction for flowering time in Chrysanthemum. Planta, 2023, 259(1. 13

[36] Sun P, Jia HX, Cheng XQ, Zhang YH, Li JB, Zhang L, Lu MZ, Zhang J, Hu JJ. Genetic architecture of leaf morphological and physiological traits in a Populus deltoides ‘Danhong’ × P. simonii ‘Tongliao1’ pedigree revealed by quantitative trait locus analysis. Tree Genet Genomes, 2020, 16(3. 45

[37] Sun YQ, Shang LG, Zhu QH, Fan LJ, Guo LB. Twenty years of plant genome sequencing: achievements and challenges. Trends Plant Sci, 2022, 27(4): 391-401.

[38] Thakur AK, Kumar P, Parmar N, Shandil RK, Aggarwal G, Gaur A, Srivastava DK. Achievements and prospects of genetic engineering in poplar: a review. New for, 2021, 52(6): 889-920.

[39] Tibbs Cortes L, Zhang ZW, Yu JM. Status and prospects of genome-wide association studies in plants. Plant Genome, 2021, 14(1. e20077

[40] Tong CF, Li HG, Wang Y, Li XR, Ou JJ, Wang DY, Xu HX, Ma C, Lang XY, Liu GX, Zhang B, Shi JS. Construction of high-density linkage maps of Populus deltoides × P. simonii using restriction-site associated DNA sequencing. PLoS ONE, 2016, 11(3. e0150692

[41] Törjék O, Kiss E, Kiss J, Kondrák M, Gyulai G, Gergácz J, Heszky L. Evaluation of genetic diversity of poplar genotypes by RAPD and AP-PCR analysis. Acta Biol Hung, 2001, 52(2–3): 345-354.

[42] Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D. The genome of black cottonwood, Populus trichocarpa (Torr & Gray). Science, 2006, 313(5793): 1596-1604.

[43] Van Soest PJ, McQueen RW. The chemistry and estimation of fibre. Proc Nutr Soc, 1973, 32(3): 123-130.

[44] Wang YX, Sun XY, Tan BY, Zhang B, Xu L, Huang MR, Wang MX. A genetic linkage map of Populus adenopoda Maxim. × P. alba L. hybrid based on SSR and SRAP markers. Euphytica, 2010, 173(2): 193-205.

[45] Wang DW, Yang L, Shi C, Li SG, Tang HY, He CZ, Cai NH, Duan AN, Gong HD. Qtl mapping for growth-related traits by constructing the first genetic linkage map in Simao pine. BMC Plant Biol, 2022, 22(1): 48.

[46] Wickham H. ggplot2. Wires Comput Stat, 2011, 3(2): 180-185.

[47] Wu WG, Zhang XF, Deng Z, An ZW, Huang HS, Li WG, Cheng H. Ultrahigh-density genetic map construction and identification of quantitative trait loci for growth in rubber tree (Hevea brasiliensis). Ind Crops Prod, 2022, 178. 114560

[48] Xia WX, Xiao ZA, Cao P, Zhang Y, Du KB, Wang N. Construction of a high-density genetic map and its application for leaf shape QTL mapping in poplar. Planta, 2018, 248(5): 1173-1185.

[49] Xu Y, Li PC, Yang ZF, Xu CW. Genetic mapping of quantitative trait loci in crops. Crop J, 2017, 5(2): 175-184.

[50] Xu HY, Wang ZX, Wang FX, Hu XR, Ma CX, Jiang HJ, Xie C, Gao YH, Ding GS, Zhao CH, Qin R, Cui DZ, Sun H, Cui F, Wu YZ. Genome-wide association study and genomic selection of spike-related traits in bread wheat. Theor Appl Genet, 2024, 137(6): 131.

[51] Yu GC, Wang LG, Han YY, He QY. Clusterprofiler: an R package for comparing biological themes among gene clusters. OMICS, 2012, 16(5): 284-287.

[52] Zhang D, Zhang Z, Yang K, Li B. Genetic mapping in (Populus tomentosa × Populus bolleana) and P. tomentosa Carr. using AFLP markers. Theor Appl Genet, 2004, 108(4): 657-662.

[53] Zhang Y, Xu H, Kong YZ, Hua JW, Tang XF, Zhuang YM, Bai Y, Zhou GK, Chai GH. Wood forming tissue-specific expression of PdSuSy and HCHL increases holocellulose content and improves saccharification in Populus. J Forestry Res, 2021, 32(4): 1681-1688.

[54] Zhang YH, Fang SZ, Tian Y, Wang LL, Lv Y. Responses of radial growth, wood density and fiber traits to planting space in poplar plantations at a lowland site. J Forestry Res, 2022, 33(3): 963-976.

[55] Zhang L, Lu DY, Ge XL, Du JJ, Wen SS, Xiang XD, Du CJ, Zhou XL, Hu JJ. Insight into growth and wood properties based on QTL and eQTL mapping in Populus deltoides ‘Danhong’ × Populus simonii ‘Tongliao1’. Ind Crops Prod, 2023, 199. 116731

[56] Zhou Y, Vales MI, Wang AX, Zhang ZW. Systematic bias of correlation coefficient may explain negative accuracy of genomic prediction. Brief Bioinform, 2017, 18(5): 744-753.

[57] Zhu CS, Gore M, Buckler ES, Yu JM. Status and prospects of association mapping in plants. Plant Genome, 2008, 1(1): 89.

[58] Zhu XL, Weng QJ, Bush D, Zhou CP, Zhao HW, Wang P, Li FG. High-density genetic linkage mapping reveals low stability of QTLs across environments for economic traits in Eucalyptus. Front Plant Sci, 2022, 13. 1099705

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Northeast Forestry University