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Drought resistance and DNA methylation of interspecific hybrids between Fraxinus mandshurica and Fraxinus americana

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Abstract

Key Message

The advantages of F1 hybrid progenies of Fraxinus mandshurica and Fraxinus americana were analyzed under drought conditions in the field and greenhouse.

Abstract

For cross-pollination trees, the optimal breeding method is hybridization. Tree heterosis is commonly present and is the main research focus in tree crossbreeding. In this study, Fraxinus mandshurica was used as female and Fraxinus americana was used as male parents to generate F1 hybrid generation. The adaptability and overwintering survival of F1 hybrids were evaluated under natural conditions. The advantages of F1 generation were analyzed under drought conditions in the field and greenhouse. The results showed that hybrid F1 generation (IH-10 and IH-15) had significantly higher growth and survival rate than the intraspecific progenies from either F. mandshurica or F. americana (MA-13 and FA-43, respectively) in the field. After 12 days of drought stress, growth, chlorophyll a and b, superoxide dismutase and peroxidase of IH-10 and IH-15 were higher than those of MA-13 and FA-43, suggesting an advantage of drought resistance for the hybrid progenies. Relationship of drought resistance and DNA methylation of interspecific hybrids was analyzed. Without drought treatment, methylation degree in the hybrid progenies (IH-10 and IH-15) was lower than that in the paternal or maternal progenies (MA-13 and FA-43). Drought stress enhanced the methylation rate in both hybrid and parental progenies, with higher increases in MA-13 and FA-43 than those in IH-10 and IH-15. Methylation in MA-13 and FA-43 mainly occurred in the full methylation of the internal cytosine, while in IH-10, methylation occurred in both full methylation of the internal cytosine and hemi-methylation of the external cytosine. These results showed that DNA methylation pattern was reconstructed in the hybrid progenies. Further analysis indicated that methylated DNA fragments were associated with growth and cell metabolism. Southern blot and transcriptional analysis showed that DNA methylation in FmaHSP70, FmaCO, FmaWRKY2 and FmaEF1A altered their gene expression. We observed that alteration of DNA methylation is closely correlated with the adaptation to the drought stress and provided epigenetic mechanisms of drought resistance in the interspecific hybridization of trees.

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References

  • Abrams MD, Mostoller SA (1995) Gas exchange, leaf structure and nitrogen in contrasting successional tree species growing in open and understory sites during a drought. Tree Physiol 15(6):361–370

    Article  PubMed  Google Scholar 

  • Adams KL (2007) Evolution of duplicate gene expression in polyploidy and hybrid plants. J Hered 98(2):136–141

    Article  CAS  PubMed  Google Scholar 

  • Amako K, Chen GX, Asada K (1994) Separate assay specific for ascorbate peroxidase and guaiacol peroxidase and for chloroplastic and cytosolic isoenzymes of ascorbate peroxidase in plants. Plant Cell Physiol 35:497–504

    CAS  Google Scholar 

  • Andersen GR, Nissen P, Nyborg J (2003) Elongation factors in protein biosynthesis. Trends Biochem Sci 28(8):434–441

    Article  CAS  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Aufsatz W, Mette M, Matzke A, Matzke M (2004) The role of MET1 in RNA-directed de novo and maintenance methylation of CG dinucleotides. Plant Mol Biol 54(6):793–804

    Article  CAS  PubMed  Google Scholar 

  • Bilichak A, Ilnystkyy Y, Hollunder J, Kovalchuk I (2012) The progeny of Arabidopsis thaliana plants exposed to salt exhibit changes in DNA methylation, histone modifications and gene expression. PLoS ONE 7(1):e30515

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Birchler JA, Yao H, Chudalayandi S, Vaiman D, Vieti RA (2010) Heterosis. Plant Cell 22(7):2105–2112

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Blum A, Ebercon A (1981) Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Sci 21:43–47

    Article  Google Scholar 

  • Boyko A, Kovalchuk I (2011) Genome instability and epigenetic modification—heritable responses to environmental stress? Curr Opin Plant Biol 14:260–266

    Article  PubMed  Google Scholar 

  • Brand MD, Affourtit C, Esteves TC, Green K, Lambert AJ, Miwa S, Pakay JL, Parker N (2004) Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic Biol Med 37:755–767

    Article  CAS  PubMed  Google Scholar 

  • Bräutigam K, Vining KJ, Lafon-Placette C et al (2013) Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecol Evol 3:399–415

    Article  PubMed Central  PubMed  Google Scholar 

  • Cao X, Jacobsen SE (2002a) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci USA 99(4):16491–16498

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cao X, Jacobsen SE (2002b) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12(13):1138–1144

    Article  CAS  PubMed  Google Scholar 

  • Cao X, Springer NM, Muszynski MG, Phillips RL, Kaeppler S, Jacobsen SE (2000) Conserved plant genes with similarity to mammalian de novo DNA methyltransferases. Proc Natl Acad Sci USA 97(9):4979–4984

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chan SW, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6(5):351–360

    Article  CAS  PubMed  Google Scholar 

  • Chen ZJ (2010) Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci 15(2):57–71

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cho EK, Hong CB (2004) Molecular cloning and expression pattern analyses of heat shock protein 70 genes from Nicotiana tabacum. J Plant Biol 47:149–159

    Article  CAS  Google Scholar 

  • Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452(7184):215–219

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • DaCosta M, Huang BR (2007) Changes in antioxidant enzyme activities and lipid peroxidation for bentgrass species in response to drought stress. J Am Soc Hortic Sci 132(3):319–326

    CAS  Google Scholar 

  • Duan Y, Qian J, Sun Y, Yi Z, Yan M (2009) Construction of methylation linkage map based on MSAP and SSR markers in Sorghum bicolor (L.). IUBMB Life 61:663–669

    Article  CAS  PubMed  Google Scholar 

  • Feng S, Jacobsen SE (2011) Epigenetic modifications in plants: an evolutionary perspective. Curr Opin Plant Biol 14:179–186

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Finnegan EJ, Peacock WJ, Dennis ES (2000) DNA methylation, a key regulator of plant development and other processes. Curr Opin Genet Dev 10(2):217–223

    Article  CAS  PubMed  Google Scholar 

  • Grant-Downton R, Dickinson H (2005) Epigenetics and its implications for plant biology. 1. The epigenetic network in plants. Ann Bot 96:1143–1164

    Article  CAS  PubMed  Google Scholar 

  • Guo M, Rupe MA, Yang X, Crasta O, Zinselmeier C, Smith OS, Bowen B (2006) Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis. Theor Appl Genet 113(5):831–845

    Article  CAS  PubMed  Google Scholar 

  • Hu LJ, Uchiyama K, Shen HL, Saito Y, Tsuda Y, Ide Y (2008) Nuclear DNA microsatellites reveal genetic variation but a lack of phylogeographical structure in an endangered species. Fraxinus mandshurica, across North-east China. Ann Bot Lond 102(2):195–205

    Article  Google Scholar 

  • Hwang CS, Rhie G, Kim ST, Kim YR, Huh WK, Baek YU, Kang SO (1999) Copper- and zinc-containing super-oxide dismutase and its gene from Candida albicans. Biochim Biophys Acta 1427:245–255

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa R, Kinoshita T (2009) Epigenetic programming: the challenge to species hybridization. Mol Plant 2(4):589–599

    Article  CAS  PubMed  Google Scholar 

  • Jackson JP, Lindroth AM, Cao X (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416(6880):556–560

    Article  CAS  PubMed  Google Scholar 

  • Jiang YW, Huang B (2001) Effects of calcium on antioxidant activities and water relations associated with heat tolerance in two cool-season grasses. J Exp Bot 52:341–349

    Article  CAS  PubMed  Google Scholar 

  • Kakutani T (2002) Epi-alleles in plants: inheritance of epigenetic information over generations. Plant Cell Physiol 43(10):1106–1111

    Article  CAS  PubMed  Google Scholar 

  • Karan R, DeLeon T, Biradar H, Subudhi PK (2012) Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. PLoS ONE 7(6):e40203

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, Jacobsen SE, Fischer RL, Kakutani T (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303(5657):521–523

    Article  CAS  PubMed  Google Scholar 

  • Kosugi H, Kikugawa K (1985) Thiobarbituric acid reaction of aldehydes and oxidized lipids in glacial acetic acid. Lipids 20(12):915–921

    Article  CAS  Google Scholar 

  • Kovalchuk I, Abramov V, Pogribny I, Kovalchuk O (2004) Molecular aspects of plant adaptation to life in the Chernobyl zone. Plant Physiol 135:357–363

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11(3):204–220

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li B, Howe GT, Wu R (1998) Developmental factors responsible for heterosis in aspen hybrids (Populus tremuloides × P. tremula. Tree Physiol 18(1):29–36

    Article  PubMed  Google Scholar 

  • Libby WJ, Stettler RF, Seitz FW (1969) Forest genetics and forest-tree breeding. Annu Rev Genet 3:469–494

    Article  Google Scholar 

  • Lima ALS, DaMatta FM, Pinheiro HA, Totola MR, Loureiro ME (2002) Photochemical responses and oxidative stress in two clones of Coffea canephora under water deficit conditions. Environ Exp Bot 47:239–247

    Article  CAS  Google Scholar 

  • Liu B, Wendel JF (2000) Retrotransposon activation followed by rapid repression in introgressed rice plants. Genome 43:874–880

    Article  CAS  PubMed  Google Scholar 

  • Lovisolo C, Schubert A (1998) Effects of water stress on vessel size and xylem hydraulic conductivity in Vitis vinifera L. J Exp Bot 49(321):693–700

    CAS  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivar differing in salinity resistance. Ann Bot 78:389–398

    Article  CAS  Google Scholar 

  • Maribel L, Dionisio-Sese Satoshi T (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    Article  Google Scholar 

  • Matzke M, Kanno T, Huettel B, Daxinger L, Matzke AJM (2007) Targets of RNA-directed DNA methylation. Curr Opin Plant Biol 10(5):1–8

    Article  Google Scholar 

  • Meir S (1992) Nondestructive assessment of chlorophyll content in watercress leaves by a tristimulus reflectance colorimeter. Postharvest Biol Technol 2:117–124

    Article  CAS  Google Scholar 

  • Meir S, Philosoph-hadas S, Aharoni N (1992) Ethylene-increased accumulation of fluorescent lipid-peroxidation products detected during senescence of parsley by a newly developed method. J Am Soc Hortic Sci 117:128–132

    CAS  Google Scholar 

  • Michalak P (2009) Epigenetic, transposon and small RNA determinants of hybrid dysfunctions. Heredity 102(1):45–50

    Article  CAS  PubMed  Google Scholar 

  • Mirouze M, Paszkowski J (2011) Epigenetic contribution to stress adaptation in plants. Curr Opin Plant Biol 14:267–274

    Article  CAS  PubMed  Google Scholar 

  • Natcheva R, Cronberg N (2007) Maternal transmission of cytoplasmic DNA in interspecific hybrids of peat mosses, Sphagnum (Bryophyta). J Evol Biol 20:1613–1616

    Article  CAS  PubMed  Google Scholar 

  • Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ (2009) Altered circadian rhythms regulate growth vigor in hybrids and allopolyploids. Nature 457(7227):327–331

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pavlopoulou A, Kossida S (2007) Plant cytosine-5 DNA methyltransferases: structure, function and molecular evolution. Genomics 90:530–541

    Article  CAS  PubMed  Google Scholar 

  • Philosoph-Hadas S, Meir S, Aharoni N (1991) Effect of wounding on ethylene biosynthesis and senescence of detached spinach leaves. Physiol Plant 83:241–246

    Article  CAS  Google Scholar 

  • Portis E, Acquadro A, Comino C, Lanteri S (2004) Analysis of DNA methylation during germination of pepper (Capsicum annuum L) seeds using ethylation-sensitive amplification polymorphism (MSAP). Plant Sci 166(1):169–178

    Article  CAS  Google Scholar 

  • Qu Z, Lanzhi L, Junyuan L, Peng W, Yu S, Tongmin M, Xingfei Z, Hu Z (2012) QTL mapping of combining ability and heterosis of agronomic traits in rice backcross recombinant inbred lines and hybrid crosses. PLoS ONE 7(1):e28463

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Queiroz CGS, Alonso A, Mares-Guia M, Magalhaes AC (1998) Chilling-induced changes in membrane fluidity and antioxidant enzyme activities in Coffea arabica L. roots. Biol Plant 41:403–413

    Article  CAS  Google Scholar 

  • Rabinowicz PD, Citek R, Budiman MA, Nunberg A, Bedell JA, Lakey N, O’Shaughnessy AL, Nascimento LU, McCombie WR, Martienssen RA (2005) Differential methylation of genes and repeats in land plants. Genome Res 15(10):1431–1440

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ramiro DA, Guerreiro-Filho O, Mazzafera P (2006) Phenol contents, oxidase activities and the resistance of coffee to the leaf miner Leucoptera coffeella. J Chem Ecol 32:1977–1988

    Article  CAS  PubMed  Google Scholar 

  • Rangwala SH, Richards EJ (2004) The value-added genome: building and maintaining genomic cytosine methylation landscapes. Curr Opin Genet Dev 14(6):686–691

    Article  CAS  PubMed  Google Scholar 

  • Rapp RA, Wendel JF (2005) Epigenetics and plant evolution. New Phytol 168:81–91

    Article  CAS  PubMed  Google Scholar 

  • Reyna-Lopez GE, Simpson J, Ruiz-Herrera J (1997) Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Mol Gen Genet 253(6):703–710

    Article  CAS  PubMed  Google Scholar 

  • Riedelsheimer C, Czedik-Eysenberg A, Grieder C, Lisec J, Technow F, Sulpice R, Altmann T, Stitt M, Willmitzer L, Melchinger AE (2012) Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nat Genet 44(2):217–220

    Article  CAS  PubMed  Google Scholar 

  • Rival A, Jaligot E, Beulé T, Finnegan EJ (2008) Isolation and expression analysis of genes encoding MET, CMT, and DRM methyltransferases in oil pa lm (Elaeis guineensis Jacq.) in relation to the ‘mantled’ somaclonal variation. J Exp Bot 59(12):3271–3281

    Article  CAS  PubMed  Google Scholar 

  • Ruiz GL, Cervera MT, Martínez-Zapater JM (2005) DNA methylation increases throughout Arabidopsis development. Planta 222(2):301–306

    Article  Google Scholar 

  • Salmon A, Ainouche ML, Wendel JF (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol Ecol 14:1163–1175

    Article  CAS  PubMed  Google Scholar 

  • Shan X, Liu Z, Dong Z, Wang Y, Chen Y, Lin X, Long L, Han F, Dong Y, Liu B (2005) Mobilization of the active MITE transposons mPing and Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). Mol Biol Evol 22(4):976–990

    Article  CAS  PubMed  Google Scholar 

  • Shepherd M, Kasem S, Lee DJ, Henry R (2008) Mapping species differences for adventitious rooting in a Corymbia torelliana × Corymbia citriodora subspecies variegata hybrid. Tree Genet Genomes 4(4):715–725

    Article  Google Scholar 

  • Shivaprasad PV, Dunn RM, Santos BACM, Bassett A, Baulcombe DC (2011) Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J 31:257–266

    Article  PubMed Central  PubMed  Google Scholar 

  • Song Y, Ji D, Li S, Wang P, Li Q, Xiang F (2012) The dynamic changes of DNA methylation and histone modifications of salt responsive transcription factor genes in soybean. PLoS ONE 7(7):e41274

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sung DY, Guy CL (2003) Physiological and molecular assessment of altered expression of Hsc70-1 in Arabidopsis: evidence for pleiotropic consequences. Plant Physiol 132:979–987

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9(6):465–476

    Article  CAS  PubMed  Google Scholar 

  • Talame V, Ozturk NZ, Bohnert HJ, Tuberosa R (2007) Barley transcript profiles under dehydration shock and drought stress treatments: a comparative analysis. J Exp Bot 58(2):229–240

    Article  CAS  PubMed  Google Scholar 

  • Tariq M, Paszkowski J (2004) DNA and histone methylation in plants. Trends Genet 20(6):244–251

    Article  CAS  PubMed  Google Scholar 

  • Tsaftaris AS, Kafka M, Polidoros A, Tani E (1999) Epigenetic changes in maize DNA and heterosis. In: Coors JG, Pandey S (eds) The genetics and exploitation of heterosis in crops. American Society of Agronomy Inc., Crop Science Society of America Inc., Madison, pp 195–203

    Google Scholar 

  • Urano K, Kurihara Y, Seki M, Shinozaki K (2010) ‘Omics’ analyses of regulatory networks in plant abiotic stress responses. Curr Opin Plant Biol 13:132–138

    Article  CAS  PubMed  Google Scholar 

  • Valledor L, Hasbún R, Meijón M, Rodríguez JL, Santamaría E, Viejo M, Berdasco M, Feito I, Fraga MF, Cañal MJ, Rodríguez R (2007) Involvement of DNA methylation in tree development and micropropagation. Plant Cell Tissue Organ Cult 91(2):75–86

    Article  CAS  Google Scholar 

  • Wang YM, Dong ZY, Zhang ZJ, Lin XY, Shen Y, Zhou D, Liu B (2005) Extensive de novo genomic variation in rice induced by introgression from wild rice (Zizania latifolia Griseb.). Genetics 170(4):1945–1956

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang Z, Zhu Y, Wang L, Liu X, Liu Y, Phillips J, Deng X (2009) A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase (BhGolS1) promoter. Planta 230(6):1155–1166

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Feng Q, Zhang M, Yang C, Sha W, Liu B (2010) Alteration of DNA methylation level and pattern in sorghum (Sorghum bicolor L.) pure-lines and inter-line F1 hybrids following low-dose laser irradiation. J Photochem Photobiol B 99(1):150–153

    Article  CAS  PubMed  Google Scholar 

  • Xiao W, Gehring M, Choi Y, Margossian L, Pu H, Harada JJ, Goldberg RB, Pennell RI, Fischer RL (2003) Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Dev Cell 5(6):891–901

    Article  CAS  PubMed  Google Scholar 

  • Xiong LZ, Xu CG, Shagi-Maroof MA, Zhang Q (1999) Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol Genet Genomics 261(3):439–446

    Article  CAS  Google Scholar 

  • Xu L, Han L, Huang B (2011) Antioxidant enzyme activities and gene expression in drought-stressed Kentucky bluegrass. J Am Soc Hortic Sci 136:247–255

    CAS  Google Scholar 

  • Yan H, Kikuchi S, Neumann P, Zhang W, Wu Y, Chen F, Jiang J (2010) Genome-wide mapping of cytosine methylation revealed dynamic DNA methylation patterns associated with genes and centromeres in rice. Plant J 63:353–365

    Article  CAS  PubMed  Google Scholar 

  • Zaefyzadeh M, Quliyev RA, Babayeva SM, Abbasov MA (2009) The effect of the interaction between genotypes and drought stress on the superoxide dismutase and chlorophyll content in durum wheat landraces. Turkish J Biol 33:1–7

    CAS  Google Scholar 

  • Zeng FS, Zhan YG, Zhao HC, Xin Y, Qi F-H, Yang CP (2010) Molecular characterization of T-DNA integration sites. Trees 24(4):753–762

    Article  CAS  Google Scholar 

  • Zhang MS, Yan HY, Zhao N, Lin XY, Pang JS, Xu KZ, Liu LX, Liu B (2007a) Epigenetic inheritance and variation of DNA methylation level and pattern in maize intra-specific hybrids. Plant Sci 172(5):930–938

    Article  Google Scholar 

  • Zhang MS, Yan HY, Zhao N, Lin XY, Pang JS, Xu KZ, Liu LX, Liu B (2007b) Endosperm-specific hypomethylation, and meiotic inheritance and variation of DNA methylation level and pattern in sorghum (Sorghum bicolor L.) interstrain hybrids. Theor Appl Genet 115(2):195–207

    Article  CAS  PubMed  Google Scholar 

  • Zhou R, Zhao H (2004) Seasonal pattern of antioxidant enzyme system in the roots of perennial forage grasses grown in alpine habitat, related to freezing tolerance. Physiol Plant 121:399–408

    Article  CAS  Google Scholar 

  • Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61–69

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was financially supported by National forestry science and technology support program (2012BAD21B0201-07), The Innovation Project of State Key Laboratory of Tree Genetics and Breeding (Northeast Forestry University) (2013B04) and the Fundamental Research Funds for the Central Universities (NO: 2572014DA04). We also thank three anonymous reviewers for many detailed and helpful comments that improved the quality of this manuscript.

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  1. State Key Laboratory of Tree Genetics and Breeding (Northeast Forestry University), Harbin, 150040, China

    Fan-Suo Zeng & Ya-Guang Zhan

  2. College of Life Science, Northeast Forestry University, Harbin, 150040, China

    Fan-Suo Zeng, Shan Zhou, Ya-Guang Zhan & Jie Dong

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  1. Fan-Suo Zeng
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Zeng, FS., Zhou, S., Zhan, YG. et al. Drought resistance and DNA methylation of interspecific hybrids between Fraxinus mandshurica and Fraxinus americana . Trees 28, 1679–1692 (2014). https://doi.org/10.1007/s00468-014-1077-z

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