Skip to main content
SpringerLink
Log in

Genetic architecture of leaf morphological and physiological traits in a Populus deltoides ‘Danhong’ × P. simonii ‘Tongliao1’ pedigree revealed by quantitative trait locus analysis

  • Original Article
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Understanding the genetic architecture of leaf morphological and physiological traits will help plant breeders develop high biomass poplar genotypes. Quantitative trait locus (QTL) studies combining next-generation sequencing techniques can advance our understanding of the genetic basis of complex traits. In this study, we measured 13 leaf morphological and physiological traits and identified quantitative trait loci (QTLs) in a Populus deltoides ‘Danhong’ × P. simonii ‘Tongliao1’ F1 population (500 progenies) using a high-density genetic map constructed by whole genome re-sequencing. This linkage map consisted of 5796 single nucleotide polymorphism (SNP) markers assigned to 19 linkage groups (LGs), spanning 2683.80 centimorgans (cM) of genetic length, with an average marker density of 0.46 cM. We identified 109 QTLs on 18 LGs for leaf morphological traits and 55 QTLs on 14 LGs for leaf physiological traits. One-hundred eight putative candidate genes were identified within the candidate genomic region. Co-expression network and gene ontology enrichment analyses suggested that these candidate genes were involved in the photosynthetic process. The differential expression patterns of the CYCLIN (Potri.015G112200) and RED CHLOROPHYLL REDUCTASE (Potri.007G043600) genes between two parents indicated their potential roles in leaf morphological and physiological traits. These findings decipher the genetic architecture of leaf morphological and physiological traits in the P. deltoides ‘Danhong’ × P. simonii ‘Tongliao1’ pedigree and provide candidate genes for future poplar genetic improvement.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agarwal G, Clevenger J, Pandey MK, Wang H, Shasidhar Y, Chu Y, Fountain JC, Choudhary D, Culbreath AK, Liu X (2018) High-density genetic map using whole-genome re-sequencing for fine mapping and candidate gene discovery for disease resistance in peanut. Plant Biotechnol J 16:1–14

    Google Scholar 

  • Bdeir R, Muchero W, Yordanov Y, Tuskan GA, Busov V, Gailing O (2017) Quantitative trait loci mapping of Populus bark features and stem diameter. BMC Plant Biol 17:224

    PubMed  PubMed Central  Google Scholar 

  • Bradshaw HD, Villar M, Watson BD, Otto KG, Stewart S, Stettler RF (1994) 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 89:167–178

    CAS  PubMed  Google Scholar 

  • Barigah TS, Saugier B, Mousseau M, Guittet J, Ceulemans R (1994) Photosynthesis, leaf area and productivity of 5 poplar clones during their establishment year. Ann Forest Sci 51:613–625

    Google Scholar 

  • Cervera MT, Storme V, Ivens B, Gusmao J, Liu BH, Hostyn V, Slycken JV, Montagu MV, Boerjan W (2001) Dense genetic linkage maps of three Populus species (Populus deltoides, P. nigra and P. trichocarpa) based on AFLP and microsatellite markers. Genetics 158:787

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ci D, Song YP, Du QZ, Tain M, Han S, Zhang DQ (2016) Variation in genomic methylation in natural population of Populus simonii is associated with leaf shape and photosynthetic traits. J Exp Bot 67:723–737

    CAS  PubMed  Google Scholar 

  • Chhetri HB, Sanz DM, Kainer D, Biswal AK, Evans LM, Chen JG, Collins C, Hunt K, Mohanty SS, Rosenstiel T, Ryon D, Winkeler K, Yang XH, Jacobson D, Mohnen D, Muchero W, Strauss SH, Tschaplinski TJ, Tuskan GA, DiFazio SP (2019) Multi-trait genome-wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits. New Phytol 1:293–309

    Google Scholar 

  • Carletti G, Carra A, Allegro G, Vietto L, Desiderio F, Bagnaresi P, Gianinetti A, Cattivelli LG, Vale GP, Nervo GP (2016) QTLs for woolly poplar aphid (Phloeomyzus passerinii L.) resistance detected in an inter-specific Populus deltoides × P. nigra mapping population, Plos one. 11:e0152569

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

    CAS  PubMed  Google Scholar 

  • Drost DR, Puranik S, Novaes E, Novaes CRDB, Dervinis C, Gailing O, Kirst M (2015) Genetical genomics of Populus leaf shape variation. BMC Plant Biol 15:166

    PubMed  PubMed Central  Google Scholar 

  • Du QZ, Xu BH, Gong CR, Yang XH, Pan W, Tian JX, Li BL, Zhang DQ (2014) Variation in growth, leaf, and wood property traits of Chinese white poplar (Populus tomentosa), a major industrial tree species in Northern China. Can J For Res 44:326–339

    Google Scholar 

  • Frewen BE, Chen THH, Howe GT, Davis J, Rohde A, Boerjan W, Bradshaw HD (2000) Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus. Genetics. 154:837–845

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Hu ZY, Deng GC, Mou HP, Xu YH, Chen L, Yang JH, Zhang MF (2017) A re-sequencing-based ultra-dense genetic map reveals a gummy stem blight resistance-associated gene in Cucumis melo. DNA Res 25:1–10

    PubMed Central  Google Scholar 

  • Huq E, Al-sady B, Hudson M, Kim CH, Apel K, Quail PH (2004) Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science. 5692:1937–1941

    Google Scholar 

  • Hackett CA, Broadfoot LB (2003) Effects of genotyping errors, missing values and segregation distortion in molecular marker data on the construction of linkage maps. Heredity. 1:33–38

    Google Scholar 

  • Induri BR, Ellis DR, Slavov GT, Yin TM, Zhang XY, Muchero W, Tuskan GA, DiFazio SP (2012) Identification of quantitative trait loci and candidate genes for cadmium tolerance in Populus. Tree Physiol 5:626–638

    Google Scholar 

  • Jorge V, Dowkiw A, Faivre-Rampant P, Bastien C (2010) Genetic architecture of qualitative and quantitative Melampsora larici-populina leaf rust resistance in hybrid poplar: genetic mapping and QTL detection. New Phytol 167:113–127

    Google Scholar 

  • Jian B, Liu WR, Xie DS, Peng QW, He XM, Lin YE, Liang ZJ (2015) High-density genetic map construction and gene mapping of pericarp color in wax gourd using specific-locus amplified fragment (SLAF) sequencing. BMC Genomics 16:1035

    Google Scholar 

  • Jiang C, Wright RJ, Woo SS, DelMonte TA, Paterson AH (2000) QTL analysis of leaf morphology in tetraploid Gossypium (cotton). Theor Appl Genet 100:409–418

    CAS  Google Scholar 

  • Juenger T, Pérez-Pérez JM, Bernal S, Micol JL (2010) Quantitative trait loci mapping of floral and leaf morphology traits in Arabidopsis thaliana: evidence for modular genetic architecture. Evol Dev 7:259–271

    Google Scholar 

  • Kosambi DD (2016) The estimation of map distance from recombination values. Springer, New York, pp 3–40

    Google Scholar 

  • Liu Z, Furnier GR (1993) Inheritance and linkage of allozymes and restriction fragment length polymorphisms in trembling aspen. J Hered 84:419–424

    CAS  Google Scholar 

  • Li BB, Lu XQ, Dou JL, Aslam A, Gao L, Zhao SJ, He N, Liu WG (2018) Construction of a high-density genetic map and mapping of fruit traits in watermelon (Citrullus Lanatus L.) based on whole-genome resequencing. Int J Mol Sci 19:3268

    PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics. 25:2078–2079

    PubMed  PubMed Central  Google Scholar 

  • Li YY, Tao HJ, Xu J, Shi ZY, Ye WJ, Wu LW, Zeng DL, Gao ZY, Guo LB (2015) QTL analysis for cooking traits of super rice with a high-density SNP genetic map and fine mapping of a novel boiled grain length locus. Plant Breed 134:535–541

    CAS  Google Scholar 

  • Ma KF, Song YP, Jiang XB, Zhang ZY, Li BL, Zhang DQ (2012) Photosynthetic response to genome methylation affects the growth of Chinese white poplar. Tree Genet Genomes 8:1407–1421

    Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Mach JM, Castillo AR, Hoogstraten R, Greenberg JT (2001) The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. P Natl Acad Sci USA 98:771–776

    CAS  Google Scholar 

  • Murchie EH, Pinto M, Horton P (2009) Agriculture and the new challenges for photosynthesis research. New Phytol 181:352–552

    Google Scholar 

  • Neale DB, Kremer A (2011) Forest tree genomics: growing resources and applications. Nat Rev Genet 12:111–122

    CAS  PubMed  Google Scholar 

  • Porth I, Klapste J, Skyba O, Lai BSK, Geraldes A, Muchero W, Tuskan GA, Douglas CJ, El Kassaby YA, Mansfield SD (2013) Populus trichocarpa cell wall chemistry and ultrastructure trait variation, genetic control and genetic correlations. New Phytol 197:777–790

    CAS  PubMed  Google Scholar 

  • Ribeiro CL, Silva CM, Drost DR, Novaes E, Novaes CRDB, Dervinis C, Kirst M (2016) Integration of genetic, genomic and transcriptomic information identifies putative regulators of adventitious root formation in Populus. BMC Plant Biol 16:66

    PubMed  PubMed Central  Google Scholar 

  • Rae AM, Robinson KM, Street NR, Taylor G (2004) Morphological and physiological traits influencing biomass productivity in short-rotation coppice poplar. Can J For Res 34:4368

    Google Scholar 

  • Street NR, Skogström O, Sjodin A, Tucker J, Rodriduez-Acosta M, Nilsson P, Jansson S, Taylor G (2010) The genetics and genomics of the drought response in Populus. Plant J 48:321–341

    Google Scholar 

  • Sun C, Niu Y, Ye X, Dong J, Hu WS, Zeng Q, Chen Z, Tian YY, Zhang J, Lu MX (2017) Construction of a high-density linkage map and mapping of sex determination and growth-related loci in the mandarin fish (Siniperca chuatsi). BMC Genomics 18:446

    PubMed  PubMed Central  Google Scholar 

  • Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T (2010) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics. 27:431–432

    PubMed  PubMed Central  Google Scholar 

  • Tuskan GA (1998) Short-rotation woody crop supply systems in the United States: what do we know and what do we need to know? Biomass Bioenergy 14:307–315

    CAS  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schei J, Sterck L, Aerts A, 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, Dejardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Eills 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, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Krist M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminien K, Nilsson O, Pereda V, Peter G, Philippe R, Poliakov GA, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tasi CJ, Uberbacher E, Unneverg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr.& gray). Science. 313:1596–1604

    CAS  PubMed  Google Scholar 

  • Tisne S, Reymond M, Vile D, Fabre J, Dauzat M, Koornneef M, Granier C (2008) Combined genetic and modeling approaches reveal that epidermal cell area and number in leaves are controlled by leaf and plant developmental processes in Arabidopsis. Plant Physiol 148:1117–1127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tian T, Liu Y, Yan HY, You Q, Yi X, Du Z, Xu WY, Su Z (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res 45:W122–W129

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Van Ooijen JW (2006) JoinMap_4: software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V., Wageningen

    Google Scholar 

  • Van Ooijen JW (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res 93:343–349

    Google Scholar 

  • Wu RL, Han YF, Hu JJ, Fang JJ, Li L, Li ML, Zeng ZB (2000) An integrated genetic map of Populus deltoides based on amplified fragment length polymorphisms. Theor Appl Genet 100:1249–1256

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Wang BW, Du QZ, Yang XH, Zhang DQ (2014) Identification and characterization of nuclear genes involved in photosynthesis in Populus. BMC Plant Biol 14:81

    PubMed  PubMed Central  Google Scholar 

  • Wu R, Bradshaw HD, J R, Stettler RF (1997) Molecular genetics of growth and development in Populus (Salicaceae). V. Mapping quantitative trait loci affecting leaf variation. Am J Bot 2:143–153

    Google Scholar 

  • Wu Y, Close TJ, Lonardi S (2008) On the accurate construction of consensus genetic maps. In: Proceedings of LSS Computational Systems. Bioinformatics Conference, 26–29 August 2008, Stanford Edited by: Peter Markstein p. 285–296

  • Wu H, Yao D, Chen Y, Yang W, Zhao W, Gao H, Tong C (2020) De novo genome assembly of Populus simonii further supports that Populus simonii and Populus trichocarpa belong to different sections, G3: Genes Genom Genet. 2:455–466

  • Wang P, Zhou GL, Yu HH, Yu SB (2011) Fine mapping a major QTL for flag leaf size and yield-related traits in rice. Theor Appl Genet 123:1319–1330

    CAS  PubMed  Google Scholar 

  • Waitt DE, Levin DA (1998) Genetic and phenotypic correlations in plants: a botanical test of Cheverud’s conjecture. Heredity. 80:310–319

    Google Scholar 

  • Wang LX, Du QZ, Xie JB, Zhou DL, Chen BB, Yang HJ, Zhang DQ (2018) Genetic variation in transcription factors and photosynthesis light-reaction genes regulates photosynthetic traits. Tree Physiol 38:1871–1885

    CAS  PubMed  Google Scholar 

  • Williams M, Lowndes L, Regan S, Beardmore T (2015) Overexpression of CYCD1;2 in activation-tagged Populus tremula × Populus alba results in decreased cell size and altered leaf morphology. Tree Genet Genomes 11:66

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Xu WY (1988) Poplar. Heilongjiang People’s Publication House

  • Yang F, Wang Y, Wang J, Deng WQ, Liao L, Li M (2011) Different eco-physiological responses between male and female Populus deltoides clones to waterlogging stress. Forest Ecol Manag 262:1963–1971

    Google Scholar 

  • Zhigunov AV, Ulianich PS, Lebedeva MV, Chang PL, Nuzhdin SV, Potokina EK (2017) Development of F1 hybrid population and the high-density linkage map for European aspen (Populus tremula L) using RADseq technology. BMC Plant Biol 17:180

    PubMed  PubMed Central  Google Scholar 

  • Zhang C, Li S, Zhao Z, Hu J, Han Y (2008) A new poplar variety Populus deltoides CL. ‘Danhong’. Sci Silvae Sin 44:1

    Google Scholar 

  • Zhang J, Li Y, Liu BB, Wang LJ, Zhang L, Hu JJ, Chen J, Zheng HQ, Lu MZ (2018) Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance. BMC Plant Biol 18:124

    PubMed  PubMed Central  Google Scholar 

  • Zhang X, Ju HW, Chung MS, Huang P, Ahn SJ, Kim CS (2011) The R-R-type MYB-like transcription factor, AtMYBL, is involved in promoting leaf senescence and modulates an abiotic stress response in Arabidopsis. Plant Cell Physiol 1:138–148

    Google Scholar 

Download references

Data archiving statement

The re-sequence data is uploaded at the National Genomics Data Center (https://bigd.big.ac.cn/gsa/) under accessions CRA002178.

Funding

This work was supported by the National Key Research and Development Program of China (2017YFD0600201), the National Natural Science Foundation of China (31570669), and the National Key Program on Transgenic Research (2018ZX08020002).

Author information

Author notes

  1. Pei Sun and Huixia Jia contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of the State Forestry and Grassland Administration, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, 100091, China

    Pei Sun, Huixia Jia, Xingqi Cheng, Yahong Zhang, Lei Zhang, Mengzhu Lu, Jin Zhang & Jianjun Hu

  2. Experimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing, 102300, China

    Jianbo Li

  3. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA

    Jin Zhang

Authors
  1. Pei Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huixia Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xingqi Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yahong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jianbo Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mengzhu Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jianjun Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jin Zhang or Jianjun Hu.

Additional information

Communicated by D. Chagné

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PNG 54 kb)

High Resolution Image (TIFF 602 kb)

ESM 2

(PNG 61 kb)

High Resolution Image (TIFF 502 kb)

ESM 3

(PDF 6488 kb)

ESM 4

(PNG 150 kb)

High Resolution Image (TIFF 1423 kb)

ESM 5

(PNG 1766 kb)

High Resolution Image (TIFF 2035 kb)

ESM 6

(PNG 1055 kb)

High Resolution Image (TIFF 1269 kb)

ESM 7

(XLSX 8 kb)

ESM 8

(XLSX 64 kb)

ESM 9

(XLSX 9 kb)

ESM 10

(XLSX 38 kb)

ESM 11

(XLSX 9 kb)

ESM 12

(XLSX 27255 kb)

ESM 13

(XLSX 11.8 kb)

ESM 14

(XLSX 24 kb)

ESM 15

(XLSX 31 kb)

ESM 16

(XLSX 2630 kb)

ESM 17

(XLSX 155 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, P., Jia, H., Cheng, X. et al. Genetic architecture of leaf morphological and physiological traits in a Populus deltoides ‘Danhong’ × P. simonii ‘Tongliao1’ pedigree revealed by quantitative trait locus analysis. Tree Genetics & Genomes 16, 45 (2020). https://doi.org/10.1007/s11295-020-01438-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-020-01438-y

Keywords

Search

Navigation