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Single nucleotide polymorphisms in two GID1 orthologs associate with growth and wood property traits in Populus tomentosa

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Abstract

Gibberellic acids (GAs) have multiple functions in various stages of plant growth and wood development, and GA receptor GIBBERELLIN INSENSITIVE DWARF 1 (GID1) is a key player in GA signaling. Here, we used association studies to examine the allelic variation within PtoGID1a and PtoGID1b associated with growth and wood properties in a natural population of Populus tomentosa. We isolated two full-length PtoGID1a and PtoGID1b cDNA by reverse transcription PCR, and both of these two genes had an open reading frame with the same length (1035 bp) and encoded a protein of 344 amino acids. Analysis of tissue-specific expression profiles indicated that these two genes had similar transcription patterns, being expressed predominantly in leaves. Nucleotide diversity and linkage disequilibrium (LD) analysis showed that PtoGID1a and PtoGID1b harbor high single nucleotide polymorphism (SNP) diversity (π Τ = 0.08237 and 0.00921, respectively) and low LD (r 2 > 0.1, within 350 and 1000 bp, respectively). SNP- and haplotype-based association tests identified that six single SNPs (Q < 0.05) and six haplotypes (P < 0.05, Q < 0.10) were significantly associated with growth and wood properties, explaining 0.99–10.28 and 3.10–5.39 % of the phenotypic variance, respectively. Therefore, isolation of PtoGID1a and PtoGID1b and dissection of their allelic polymorphisms open an avenue to understand the regulation of PtoGID1 in the growth and wood formation in trees.

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References

  • Akey J, Jin L, Xiong M (2001) Haplotypes vs single marker linkage disequilibrium tests: what do we gain? Eur J Hum Genet 9:291–300

    Article  CAS  PubMed  Google Scholar 

  • Aleman L, Kitamura J, Abdel-mageed H et al (2008) Functional analysis of cotton orthologs of GA signal transduction factors GID1 and SLR1. Plant Mol Biol 68:1–16

    Article  CAS  PubMed  Google Scholar 

  • Barrett LW, Fletcher S, Wilton SD (2012) Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements. Cell Mol Life Sci 69:3613–3634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beaulieu J, Doerksen T, Boyle B, Clement S, Deslauriers M et al (2011) Association genetics of wood physical traits in the conifer white spruce and relationships with gene expression. Genetics 188:197–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bourgain C, Hoffjan S, Nicolae R, Newman D et al (2003) Novel case-control test in a founder population identifies P-selectin as an atopy-susceptibility locus. Am J Hum Genet 73:612–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bradshaw HD, Ceulemans R, Davis J, Stettler R (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 

  • Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9:49–56

    Article  CAS  PubMed  Google Scholar 

  • Chandler PM, Marion-Poll A, Ellis M, Gubler F (2002) Mutants at the Slender1 locus of ‘Himalaya’ barley: molecular and physiological characterization. Plant Physiol 129:181–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandler PM, Harding CA, Ashton AR, Mulcair MD, Dixon NE, Mander LN (2008) Characterization of gibberellin receptor mutants of barley (Hordeum vulgare L.). Mol Plant 1:285–294

    Article  CAS  PubMed  Google Scholar 

  • Du Q, Wang B, Wei Z, Zhang D, Li B (2012) Genetic diversity and population structure of Chinese white poplar (Populus tomentosa) revealed by SSR markers. J Hered 103:853–862

    Article  PubMed  Google Scholar 

  • Du Q, Xu B, Pan W, Gong C (2013) Allelic variation in a cellulose synthase gene (PtoCesA4) associated with growth and wood properties in Populus tomentosa. G3: Genes Genomes Genetics 3:2069–2084

    Article  PubMed  PubMed Central  Google Scholar 

  • Du Q, Wang L, Zhou D, Yang H, Gong C et al (2014a) Allelic variation within the S-adenosyl-L-homocysteine hydrolase gene family is associated with wood properties in Chinese white poplar(Populus tomentosa). BMC Genet 15(Suppl 1):S4

    Article  PubMed  PubMed Central  Google Scholar 

  • Du Q, Xu B, Gong C, Yang X, Pan W, Tian J, Li B, Zhang D (2014b) Variation in growth, leaf and wood-property traits of Chinese white poplar (Populus tomentosa Carr.), a major industrial tree species in Northern China. Can J For Res 44:326–339

    Article  Google Scholar 

  • Eckert AJ, Bower AD, Wegrzyn JL, Pande B, Jermstad KD et al (2009) Association genetics of coastal Douglas fir (Pseudotsuga menziesii var. menziesii, Pinaceae). I. Cold hardiness related traits. Genetics 182:1289–1302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ehrenreich IM, Hanzawa Y, Chou L, Roe JL, Kover PX et al (2009) Candidate gene association mapping of Arabidopsis flowering time. Genetics 183:325–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Griffiths J, Murase K, Rieu I et al (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18:3399–3414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hill W-G, Robertson A (1968) Linkage disequilibrium in finite population. Theor Appl Genet 38:226–231

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hirano K, Nakajima M, Asano K et al (2007) The GID1-mediated gibberellin perception mechanism is conserved in the lycophyte Selaginella moellendorffii but not in the bryophyte Physcomitrella patens. Plant Cell 19:3058–3079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirano K, Ueguchi-Tanaka M, Matsuoka M (2008) GID1-mediated gibberellin signaling in plants. Plant Cell 13:192–199

    CAS  Google Scholar 

  • Huang Z (1992) The study on the climatic regionalization of the distributional region of Populus tomentosa. J Beijing For Univ 14:26–32

    CAS  Google Scholar 

  • Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Matsuoka M, Yamaguchi J (2001) Slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height regulating gene GAI/RGA/RHT/D8. Plant Cell 13:999–1010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Israelsson M, Sundberg B, Moritz T (2005) Tissue-specific localization of gibberellins and expression of gibberellin-biosynthetic and signaling genes in wood forming tissues in aspen. Plant J 44:494–504

    Article  CAS  PubMed  Google Scholar 

  • Iuchi S, Suzuki H, Kim Y-C, Iuchi A et al (2007) Multiple loss of-function of Arabidopsis gibberellin receptor AtGID1s completely shuts down a gibberellin signal. Plant J 50:958–966

    Article  CAS  PubMed  Google Scholar 

  • Kimchi-Sarfati C, Oh JM, Kim IW, Sauna ZE, Calcagno AM et al (2007) A “silent” polymorphism in the MDR1 gene changes substrate specificity. Science 315:525–528

    Article  Google Scholar 

  • Li A, Yang W, Li S et al (2013) Molecular characterization of three GIBBERELLIN-INSENSITIVE DWARF1 homologous genes in hexaploid wheat. J Plant Physiol 170:432–443

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1452–1452

    Article  Google Scholar 

  • Maurano M, Humbert R, Rynes E, Thurman R, Haugen E et al (2012) Systematic localization of common disease-associated variation in regulatory DNA. Science 337:1190–1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mauriat M, Moritz T (2009) Analyses of GA20ox- and GID1-over-expressing aspen suggest that gibberellins play two distinct roles in wood formation. Plant J 58:989–1003

    Article  CAS  PubMed  Google Scholar 

  • Murase K, Hirano Y, Sun T, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:459–464

    Article  CAS  PubMed  Google Scholar 

  • Nakajima M, Shimada A, Takashi Y et al (2006) Identification and characterization of Arabidopsis gibberellin receptors. Plant J 46:880–889

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Olszewski N, Sun T, Gubler F (2002) Gibberellin signaling biosynthesis, catabolism, and response pathways. Plant Cell 14:S61–S80

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively. Gene Dev 11:3194–3205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porth I, Klápště J, Skyba O, Lai BS, Geraldes A et al (2013) Populus trichocarpa cell wall chemistry and ultrastructure trait variation, genetic control, and genetic correlations. New Phytol 197:777–790

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ritland K (1996) Estimators for pairwise relatedness and individual inbreeding coefficients. Genet Res 67:175–185

    Article  Google Scholar 

  • Roa-Rodrigues C (2003) Promoters used to regulate gene expression. CAMBIA Intellectual Property, Canberra

    Google Scholar 

  • Schimleck LR, Kube PS, Raymond CA (2004) Genetic improvement of Kraft pulp yield in Eucalyptus nitens using cellulose content determined by near infrared spectroscopy. Can J For Res 34:2363–2370

    Article  CAS  Google Scholar 

  • Shimada A, Ueguchi-Tanaka M, Nakatsu T, Nakajima M (2008) Structural basis for gibberellin recognition by its receptor GID1. Nature 456:520–523

    Article  CAS  PubMed  Google Scholar 

  • Southerton SG, MacMillan CP, Bell JC, Bhuiyan N, Downes G et al (2010) Association of allelic variation in xylem genes with wood properties in Eucalyptus nitens. Austral For 73:259–264

    Article  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genome wide studies. Proc Natl Acad Sci U S A 100:9440–9445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Storey JD, Taylor JE, Siegmund D (2004) Strong control, conservative point estimation and simultaneous conservative consistency of false discovery rates: a unified approach. J R Stat Soc Ser B 66:187–205

    Article  Google Scholar 

  • Su Z, Hao C, Wang L, Dong Y, Zhang X (2011) Identification and development of a functional marker of TaGW2 associated with grain weight in bread wheat (Triticum aestivum L.). Theor Appl Genet 122:211–223

    Article  CAS  PubMed  Google Scholar 

  • Sun T (2011) The molecular mechanism and evolution of the GA–GID1–DELLA signaling module in plants. Curr Biol 21:R338–R345

    Article  CAS  PubMed  Google Scholar 

  • Sun T, Gubler F (2004) Molecular mechanism of gibberellins signaling in plants. Annu Rev Plant Biol 55:197–223

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thumma BR, Matheson BA, Zhang D, Meeske C, Meder R et al (2009) Identification of a cis-acting regulatory polymorphism in a Eucalypt cobra-like gene affecting cellulose content. Genetics 183:1153–1164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian J, Du Q, Chang M, Zhang D (2012) Allelic variation in PtGA20Ox associates with growth and wood properties in Populus spp. PLoS One 7(12):e53116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian J, Chang M, Du Q, Xu B, Zhang D (2014a) Single-nucleotide polymorphisms in PtoCesA7 and their association with growth and wood properties in Populus tomentosa. Mol Gen Genomics 289:439–455

    Article  CAS  Google Scholar 

  • Tian J, Du Q, Xu B, Li B, Zhang D (2014b) Single-nucleotide polymorphisms in the 5′ UTR of UDP-glucose dehydrogenase (PtUGDH) associate with wood properties in Populus tomentosa. Tree Genet Genomes 10:339–354

    Article  Google Scholar 

  • Ueguchi-Tanaka M, Ashikari M, Nakajima M et al (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellins. Nature 437:693–698

    Article  CAS  PubMed  Google Scholar 

  • Ueguchi-Tanaka M, Nakajima M, Katoh E et al (2007a) Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19:2140–2155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueguchi-Tanaka M, Nakajima M, Motoyuki A, Matsuoka M (2007b) Gibberellin receptor and its role in gibberellin signaling in plants. Annu Rev Plant Biol 58:183–198

    Article  CAS  PubMed  Google Scholar 

  • Voegele A, Linkies A, Muller K, Leubner-Metzger G (2011) Members of the gibberellin receptor gene family GID1(GIBBERELLIN INSENSITIVE DWARF1) play distinct roles during Lepidium sativum and Arabidopsis thaliana seed germination. J Exp Bot 62:5131–5147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:188–193

    Article  Google Scholar 

  • Wegrzyn JL, Eckert AJ, Choi M, Lee JM, Stanton BJ et al (2010) Association genetics of traits controlling lignin and cellulose biosynthesis in black cottonwood (Populus trichocarpa, Salicaceae) secondary xylem. New Phytol 188:515–532

    Article  CAS  PubMed  Google Scholar 

  • Yang XH, Yan JB, Shah T, Warburton ML, Li Q et al (2010) association mapping panel for quantitative trait loci dissection. Theor Appl Genet 121:417–431

  • Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    Article  CAS  PubMed  Google Scholar 

  • Zaykin DV, Westfall PH, Young SS, Karnoub MA, Wagner MJ, Ehm MG (2002) Testing association of statistically inferred haplotypes with discrete and continuous traits in samples of unrelated individuals. Hum Hered 53:79–91

    Article  PubMed  Google Scholar 

  • Zhang D, Zhang Z (2005) Single nucleotide polymorphisms discovery and linkage disequilibrium. For Studies China 7:1–14

    Article  Google Scholar 

  • Zhang DQ, Zhang ZY, Yang K (2006) QTL analysis of growth and wood chemical content traits in an interspecific backcross family of white poplar (Populus tomentosa × P. bolleana) × P. tomentosa. Can J For Res 36:2015–2023

    Article  CAS  Google Scholar 

  • Zhang D, Du Q, Xu B, Zhang Z, Li B (2010) The actin multigene family in Populus: organization, expression and phylogenetic analysis. Mol Gen Genomics 284:105–119

    Article  CAS  Google Scholar 

  • Zhao K, Aranzana MJ, Kim S, Lister C et al (2007) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3:e4

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu Z (1992) Collection, conservation and utilization of plus tree resources of Populus tomentosa in China. J Beijing For Univ 14:1–25

    Google Scholar 

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Acknowledgments

This work was supported by the National “863” Plan Project (No. 2013AA102702) and the Project of the National Natural Science Foundation of China (No. 31670333).

Data archiving statement

Sequence data from this article has been deposited in the GenBank Data Library under the accession Nos. KU161176–KU161220 and KU161221–KU161265.

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Authors and Affiliations

  1. National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, People’s Republic of China

    Haijiao Yang, Xiaohui Yang, Longxin Wang, Chenrui Gong, Beibei Chen, Qingzhang Du & Deqiang Zhang

  2. Key Laboratory Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, People’s Republic of China

    Haijiao Yang, Xiaohui Yang, Longxin Wang, Chenrui Gong, Beibei Chen, Qingzhang Du & Deqiang Zhang

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  1. Haijiao Yang
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Correspondence to Deqiang Zhang.

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Communicated by P. Ingvarsson

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Fig. S1

Putative amino acid sequence alignment of PtoGID1a and PtoGID1b with other plant GID1s. Numbers on the right represent the positions of amino acid residues in each protein. Sequences in the gray boxes refer to the highly conserved domains HGG and GXGSXG of GID1 and HSL. The arrows show the three catalytic centers S (Ser), D (Asp), and H (His) of HSL family. Thirteen binding domains for GA-GID1-DELLA (TWVLIS, LDR, FFHGGSF, HS, IYD, YRR, DGW, GDSSGGNI, GNI, MF, LDGKYF, WYW, and GFY) are indicated in bold font. (GIF 449 kb)

High resolution image (TIFF 716 kb)

Fig. S2

Pairwise linkage disequilibrium (r 2) between SNP markers. (a) Thirteen distinct haplotype blocks within PtoGID1a. (b) Four distinct haplotype blocks within PtoGID1b. The pairwise r 2 values are shown in color. Within each block, LD among the SNPs was high (r 2 > 0.75). Dashed lines indicate the physical location of the SNPs within PtoGID1a and PtoGID1b. (GIF 312 kb)

High resolution image (TIFF 80 kb)

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Yang, H., Yang, X., Wang, L. et al. Single nucleotide polymorphisms in two GID1 orthologs associate with growth and wood property traits in Populus tomentosa . Tree Genetics & Genomes 12, 109 (2016). https://doi.org/10.1007/s11295-016-1070-3

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