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Detection of quantitative trait loci influencing growth trajectories of adventitious roots in Populus using functional mapping

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Abstract

The capacity to root from cuttings is a key factor for the mass deployment of superior genotypes in clonal forestry. We studied the genetic basis of rooting capacity by mapping quantitative trait loci (QTLs) that control growth rate and form of root traits in a full-sib family of 93 hybrids derived from an interspecific cross between two Populus species, P. deltoides and P. euramericana. The hybrid family was typed for different marker systems (including SSRs, AFLPs, RAPDs, ISSRs, and SNPs), leading to the construction of two linkage maps based on the female P. deltoides (D map) and male P. euramericana (E map) with a pseudotestcross mapping strategy. The two maps were scanned by functional mapping to detect QTLs that control early growth trajectories of two rooting traits, maximal single-root length and the total number of roots per cutting, measured at five time points in water culture. Of the six QTLs detected for these two growth traits, only one is segregating in P. deltoides with poor rooting capacity, while the other five are segregating in P. euramericana showing good rooting capacity. Tests with functional mapping suggest different developmental patterns of the genetic effects of these root QTLs in time course. Five QTLs were detected to change their effects on root growth trajectories with time, whereas one detected to affect root growth consistently in time course. Knowledge about the genetic and developmental control mechanisms of root QTLs will have important implications for the genetic improvement of vegetative propagation traits in Populus.

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References

  • Borralhon MG, Willson PJ (1994) Inheritance of initial survival and rooting ability in Eucalyptus globulus Labill. stem cutting. Silvae Genet 43:238–242

    Google Scholar 

  • Bradshaw HD, Stettler RF (1995) Molecular genetics of growth and development in Populus. IV. Mapping QTLs with large effects on growth, form, and phenology traits in a forest Tree. Genetics 139:963–973

    PubMed  CAS  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  Google Scholar 

  • Bradshaw JHD, Ceulemans R, Davis J, Stettler RF (2000) Emerging model systems in plant biology: poplar (Populus) as a model forest Tree. J Plant Growth Regul 19:306–313

    Article  CAS  Google Scholar 

  • Cervera MT, Storme V, Ivens B, Gusmao J, Liu BH, Hostyn V, Van Slycken J, Van Montagu M, 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 158:787–809

    PubMed  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Emebiri LC, Devey ME, Matheson AC, Slee MU (1998) Age-related changes in the expression of QTLs for growth in radiata pine seedlings. Theor Appl Genet 97:1053–1061

    Article  CAS  Google Scholar 

  • Frary A, Nesbitt TC, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Gerber S, Rodolphe F (1994) An estimation of the genome length of maritime pine (Pinus pinaster Ait). Theor Appl Genet 88:289–292

    Google Scholar 

  • Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137

    PubMed  CAS  Google Scholar 

  • Han KH, Bradshaw HD, Gordon MP (1994) Adventitious root and shoot regeneration in vitro is under major gene control in an F2 family of hybrid poplar (Populus trichocarpa×P. deltoides). Forest. Genetics 1:139–146

    Google Scholar 

  • Han ZM, Yin TM, Li CD, Huang MR, Wu RL (2000) Host effect on genetic variation of Marssonina brunnea pathogenic to poplars. Theor Appl Genet 100:614

    Article  CAS  Google Scholar 

  • Hulbert SH, Ilott TW, Legg EJ, Lincoln SE, Lander ES, Michelmore RW (1988) Genetic analysis of the fungus, Bremia lactucae, using restriction fragment length polymorphisms. Genetics 120:947–958

    PubMed  CAS  Google Scholar 

  • Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458

    Article  PubMed  CAS  Google Scholar 

  • Jorge V, Dowkiw A, Faivre-Rampant P, Bastien C (2005) 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

    Article  PubMed  CAS  Google Scholar 

  • Kaya Z, Sewell MM, Neale DB (1999) Identification of quantitative trait loci influencing annual height- and diameter-increment growth in loblolly pine (Pinus taeda L.). Theor Appl Genet 98:586–592

    Article  CAS  Google Scholar 

  • Kirkpatrick M, Heckman N (1989) A quantitative genetic model for growth, shape, reaction norms, and other infinite-dimensional characters. J Math Biol 27:429–450

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    PubMed  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Lerceteau E, Szmidt A, Andersson B (2001) Detection of quantitative trait loci in Pinus sylvestris L. across years. Euphytica 121:117–122

    Article  Google Scholar 

  • Lin M, Wu R (2006) A joint model for nonparametric functional mapping of longitudinal trajectory and time-to-event. Bioinformatics 7:138

    Article  PubMed  Google Scholar 

  • Lincoln SE, Lander ES (1992) Systematic detection of errors in genetic linkage data. Genomics 14:604–610

    Article  PubMed  CAS  Google Scholar 

  • Ma C-X, Casella G, Wu R (2002) Functional mapping of quantitative trait loci underlying the character process: a theoretical framework. Genetics 161:1751–1762

    PubMed  Google Scholar 

  • Mauricio R (2005) Ontogenetics of QTL: the genetic architecture of trichome density over time in Arabidopsis thaliana. Genetica 123:75–85

    Article  PubMed  Google Scholar 

  • Meyer K (2000) Random regressions to model phenotypic variation in monthly weights of Australian beef cows. Livest Prod Sci 65:19–38

    Article  Google Scholar 

  • Rieseberg LH, Carney SE (1998) Plant hybridization. New Phytol 140:599–624

    Article  Google Scholar 

  • Rönnberg-Wästljung AC, Glynn C, Weih M (2005) QTL analyses of drought tolerance and growth for a Salix dasyclados × Salix viminalis hybrid in contrasting water regimes. Theor Appl Genet 110:537–549

    Article  PubMed  Google Scholar 

  • SAS/STAT (1996) User's guide, vols 1 and 2, version 6, 4th edn. SAS Institute, Cary, NC

    Google Scholar 

  • Schreiner EJ (1970) Genetics of eastern cottonwood. USDA Forest Service, Research Paper WO-11

  • Smulders MJM, Van Der Schoot J, Arens P, Vosman B (2001) Trinucleotide repeat microsatellite markers for black poplar (Populus nigra L.). Mol Ecol Notes 1:188–190

    Article  CAS  Google Scholar 

  • Stettler RF, Bradshaw HD, Heilman PE (1996) Biology of Populus and its implications for management and conservation. NRC Research Press, National Research Council of Canada, Ottawa, Ont

    Google Scholar 

  • Taylor G (2002) Populus: Arabidopsis for forestry. Do we need a model tree? Ann Bot 90:681–689

    Article  PubMed  CAS  Google Scholar 

  • 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, Dejardin 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, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst 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, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, 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, 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 (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA, DiFazio SP, Teichmann T (2004a) Poplar genomics is getting popular: the impact of the poplar genome project on tree research. Plant Biol 6:2–4

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA, Gunter LE, Yang ZK, Yin T, Sewell MM, DiFazio SP (2004b) Characterization of microsatellites revealed by genomic sequencing of Populus trichocarpa. Can J For Res 34:85–93

    Article  CAS  Google Scholar 

  • van der Schoot J, Pospíšková M, Vosman B, Smulders MJM (2000) Development and characterization of microsatellite markers in black poplar (Populus nigra L.). Theor Appl Genet 101:317

    Article  Google Scholar 

  • Verhaegen D, Plomion C, Gion JM, Poitel M, Costa P, Kremer A (1997) Quantitative trait dissection analysis in Eucalyptus using RAPD markers: 1. Detection of QTL in interspecific hybrid progeny, stability of QTL expression across different ages. Theor Appl Genet 95:597–608

    Article  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Heredity 93:77–78

    Article  CAS  Google Scholar 

  • Wu R, Lin M (2006) Functional mapping—how to map and study the genetic architecture of dynamic complex traits. Nat Rev Genet 7:229–237

    Article  PubMed  CAS  Google Scholar 

  • Wu R, Ma C-X, Lin M, Wang Z, Casella G (2004) Functional mapping of quantitative trait loci underlying growth trajectories using a transform-both-sides logistic model. Biometrics 60:729–738

    Article  PubMed  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

    Article  CAS  Google Scholar 

  • Wullschleger SD, Jansson S, Taylor G (2002) Genomics and forest biology: Populus emerges as the perennial favorite. Plant Cell 14:2651–2655

    Article  PubMed  CAS  Google Scholar 

  • Yang R, Tian Q, Xu S (2006) Mapping quantitative trait loci for longitudinal traits in line crosses. Genetics 173:2339–2356

    Article  PubMed  CAS  Google Scholar 

  • Yin T, Huang M, Wang M, Zhu LH, Zeng ZB, Wu R (2001) Preliminary interspecific genetic maps of the Populus genome constructed from RAPD markers. Genome 44:602–609

    Article  PubMed  CAS  Google Scholar 

  • Yin T, Zhang X, Huang M, Wang M, Zhuge Q, Tu S, Zhu LH, Wu R (2002) Molecular linkage maps of the Populus genome. Genome 45:541–555

    Article  PubMed  CAS  Google Scholar 

  • Yin TM, DiFazio SP, Gunter LE, Riemenschneider D, Tuskan GA (2004) Large-scale heterospecific segregation distortion in Populus revealed by a dense genetic map. Theor Appl Genet 109:451–463

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Zhang L, Zhuge Q, Wang MX, Huang MR (2004a) A rapid and simple method of total DNA extraction from tree. Journal of Nanjing Forestry University 28:13–16

    Google Scholar 

  • Zhang B, Zhou Y, Zhang L, Zhuge Q, Wang M-X, Huang M-R (2005) Identification and validation of single nucleotide polymorphisms in poplar using publicly expressed sequence tags. J Integr Plant Biol 47:1493–1499

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zhang ZZ, Xue SX, Sun W, Zhang XT (1999) The effect of the reproduction by sprout of the stump division and the planting trees of poplar I-69. Journal of Jiangsu Forestry Science & Technology 26:23–25

    Google Scholar 

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Acknowledgements

We thank the two anonymous reviewers for their constructive comments on this manuscript. This work was partially supported by the National Natural Science Foundation of China (grant nos. 30671705 and 30872051) and NSF grant (no. 0540745).

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Correspondence to Bo Zhang.

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Communicated by W. Boerjan

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Zhang, B., Tong, C., Yin, T. et al. Detection of quantitative trait loci influencing growth trajectories of adventitious roots in Populus using functional mapping. Tree Genetics & Genomes 5, 539–552 (2009). https://doi.org/10.1007/s11295-009-0207-z

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