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Transcript abundance patterns of Populus C-repeat binding factor2 orthologs and genetic association of PsCBF2 allelic variation with physiological and biochemical traits in response to abiotic stress

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Abstract

Main conclusion

We conducted a candidate gene-based approach to search for genetic associations between 10 SNPs in PsCBF2 and 10 abiotic stress-related traits.

The increasing incidence of abiotic stresses and the limitations of available treatments, particularly in trees, highlight the need to improve our understanding of the mechanisms of stress responses. In Arabidopsis, C-repeat binding factor 2 (CBF2) plays an important role in freezing tolerance and cold acclimation. Here, we isolated orthologs of CBF2 from five Populus species. Expression profiling revealed that the Populus CBF2s were preferentially induced in response to cold, with CBF2 transcript abundances ranging from 5.4- to 62-fold higher than in unstressed controls of the corresponding species. In addition, we used a candidate gene-based approach in Populus simonii Carr. to identify single nucleotide polymorphisms (SNPs) in PsCBF2 associated with physiological and biochemical traits. PsCBF2 showed high nucleotide diversity (π T = 0.00549, θ w = 0.01406) and low average linkage disequilibrium (r 2 = 0.061). Association studies in 528 individuals of an association population showed that nine SNPs (false discovery rate Q < 0.10) and one haplotype (Q < 0.10) were significantly associated with differences in four physiological and biochemical traits (P < 0.005), with each marker explaining 1.31–5.87 % of the total variance in the corresponding trait. PsCBF2 transcript levels differed significantly in abundance among genotypic classes for most of the significant SNPs. Identification of these significant associations will help reveal the molecular basis of physiological differences and provide a starting point for marker-assisted selection for traits involved in stress tolerance in P. simonii.

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Abbreviations

ABA:

Abscisic acid

AP2/ERF:

APETALA2/ethylene-responsive element binding factor (ERF)

CAT:

Catalase

CBF:

C-repeat binding factor

DRE/CRT:

Dehydration-responsive element and C-repeat motif

DREBs:

DRE binding proteins

LD:

Linkage disequilibrium

MAS:

Marker-assisted selection

ORF:

Open reading frame

QTLs:

Quantitative trait loci

ROS:

Reactive oxygen species

SNPs:

Single nucleotide polymorphisms

TFs:

Transcription factors

References

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Benedict C, Skinner JS, Meng R, Chang Y, Bhalerao R, Huner NP, Finn CE, Chen TH, Hurry V (2006) The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant Cell Environ 29:1259–1272

    Article  CAS  PubMed  Google Scholar 

  • Bestwick CS, Brown IR, Mansfield JW (1998) Localized changes in peroxidase activity accompany hydrogen peroxide generation during the development of a nonhost hypersensitive reaction in lettuce. Plant Physiol 118:1067–1078

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bichile LS (1994) Malondialdehyde: a marker of lipid peroxidation. J Assoc Physicians India 42:769

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Brown GR, Bassoni DL, Gill GP, Fontana JR, Wheeler NC, Megraw RA, Davis MF, Sewell MM, Tuskan GA, Neale DB (2003) Identification of quantitative trait loci influencing wood property traits in loblolly pine (Pinus taeda L.) III. QTL verification and candidate gene mapping. Genetics 164:1537–1546

    CAS  PubMed Central  PubMed  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 

  • Cervera MT, Storme V, Soto A, Ivens B, Van Montagu M, Rajora OP, Boerjan W (2005) Intraspecific and interspecific genetic and phylogenetic relationships in the genus Populus based on AFLP markers. Theor Appl Genet 111:1440–1456

    Article  CAS  PubMed  Google Scholar 

  • Champ KI, Febres VJ, Moore GA (2007) The role of CBF transcriptional activators in two Citrus species (Poncirus and Citrus) with contrasting levels of freezing tolerance. Physiol Plant 129:529–541

    Article  CAS  Google Scholar 

  • Chappelka AH, Freer-Smith PH (1995) Predisposition of trees by air pollutants to low temperatures and moisture stress. Environ Pollut 87:105–117

    Article  CAS  PubMed  Google Scholar 

  • Choi DW, Rodriguez EM, Close TJ (2002) Barley Cbf3 gene identification, expression pattern, and map location. Plant Physiol 129:1781–1787

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Csiszar J, Galle A, Horvath E, Dancso P, Gombos M, Vary Z, Erdei L, Gyorgyey J, Tari I (2012) Different peroxidase activities and expression of abiotic stress-related peroxidases in apical root segments of wheat genotypes with different drought stress tolerance under osmotic stress. Plant Physiol Biochem 52:119–129

    Article  CAS  PubMed  Google Scholar 

  • Dehghan S, Sadeghi M, Poppel A, Fischer R, Lakes-Harlan R, Kavousi HR, Vilcinskas A, Rahnamaeian M (2014) Differential inductions of phenylalanine ammonia-lyase and chalcone synthase during wounding, salicylic acid treatment, and salinity stress in safflower, Carthamus tinctorius. Biosci Rep 34:273–282. doi:10.1042/BSR20140026

    Article  CAS  Google Scholar 

  • Diamant S, Eliahu N, Rosenthal D, Goloubinoff P (2001) Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 276:39586–39591

    Article  CAS  PubMed  Google Scholar 

  • Eckert AJ, Wegrzyn JL, Pande B, Jermstad KD, Lee JM, Liechty JD, Tearse BR, Krutovsky KV, Neale DB (2009) Multilocus patterns of nucleotide diversity and divergence reveal positive selection at candidate genes related to cold hardiness in coastal Douglas Fir (Pseudotsuga menziesii var. menziesii). Genetics 183:289–298

    Article  PubMed Central  PubMed  Google Scholar 

  • Ferreira S, Batista D, Serrazina S et al (2009) Morphogenesis induction and organogenic nodule differentiation in Populus euphratica Oliv. leaf explants. Plant Cell Tiss Organ Cult 96:35–43

    Article  Google Scholar 

  • Gao MJ, Allard G, Byass L, Flanagan AM, Singh J (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol Biol 49:459–471

    Article  CAS  PubMed  Google Scholar 

  • Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442

    Article  CAS  PubMed  Google Scholar 

  • Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54:767–781

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Martinez SC, Ersoz E, Brown GR, Wheeler NC, Neale DB (2006) DNA sequence variation and selection of tag single-nucleotide polymorphisms at candidate genes for drought-stress response in Pinus taeda L. Genetics 172:1915–1926

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gonzalez-Martinez SC, Wheeler NC, Ersoz E, Nelson CD, Neale DB (2007) Association genetics in Pinus taeda L. I. Wood property traits. Genetics 175:399–409

    Article  PubMed Central  PubMed  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 

  • Hegedüs A, Erdei S, Horváth G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci 160:1085–1093

    Article  PubMed  Google Scholar 

  • Huttley GA, Smith MW, Carrington M, O’Brien SJ (1999) A scan for linkage disequilibrium across the human genome. Genetics 152:1711–1722

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127:910–917

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    Article  CAS  PubMed  Google Scholar 

  • Jebara S, Jebara M, Limam F, Aouani ME (2005) Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. J Plant Physiol 162:929–936

    Article  CAS  PubMed  Google Scholar 

  • Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012) The Arabidopsis information resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40:D1202–D1210

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li SW, Zhang ZY, Luo JM, Zhang HC, Pu YS, An XM (2005) Progress and strategies in cross breeding of poplars in China. For Stud China 7:54–60

    Article  Google Scholar 

  • Li JT, Wang N, Xin HP, Li SH (2013) Overexpression of VaCBF4, a transcription factor from Vitis amurensis, improves cold tolerance accompanying increased resistance to drought and salinity in Arabidopsis. Plant Mol Biol Rep 31:1518–1528

    Article  CAS  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Llorente F, Lopez-Cobollo RM, Catala R, Martinez-Zapater JM, Salinas J (2002) A novel cold-inducible gene from Arabidopsis, RCI3, encodes a peroxidase that constitutes a component for stress tolerance. Plant J 32:13–24

    Article  CAS  PubMed  Google Scholar 

  • Madhava Rao KV, Sresty TV (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  CAS  PubMed  Google Scholar 

  • Maestrini P, Cavallini A, Rizzo M, Giordani T, Bernardi R, Durante M, Natali L (2009) Isolation and expression analysis of low temperature-induced genes in white poplar (Populus alba). J Plant Physiol 166:1544–1556

    Article  CAS  PubMed  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  CAS  PubMed  Google Scholar 

  • Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119:463–470

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Navarro M, Marque G, Ayax C, Keller G, Borges JP, Marque C, Teulieres C (2009) Complementary regulation of four Eucalyptus CBF genes under various cold conditions. J Exp Bot 60:2713–2724

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325–330

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T, Sakakibara H, Schmulling T, Tran LS (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23:2169–2183

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Novillo F, Alonso JM, Ecker JR, Salinas J (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 101:3985–3990

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA 94:7076–7081

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Phimchan P, Chanthai S, Bosland PW, Techawongstien S (2014) Enzymatic changes in phenylalanine ammonia-lyase, cinnamic-4-hydroxylase, capsaicin synthase, and peroxidase activities in Capsicum under drought stress. J Agric Food Chem 62:7057–7062

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Donnelly P (2001) Case-control studies of association in structured or admixed populations. Theor Popul Biol 60:227–237

    Article  CAS  PubMed  Google Scholar 

  • Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki K (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45:1042–1052

    Article  CAS  PubMed  Google Scholar 

  • Rahman MH, Rajora OP (2002) Microsatellite DNA fingerprinting, differentiation, and genetic relationships of clones, cultivars, and varieties of six poplar species from three sections of the genus Populus. Genome 45:1083–1094

    Article  CAS  PubMed  Google Scholar 

  • Rajinder SD, Pamela LP, Trevor AT (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreases levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Sakuma Y, Liua Q, Dubouzeta JG, Abea H, Shinozakib K, Yamaguchi-Shinozakia K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Ballesta MT, Zacarias L, Granell A, Lafuente MT (2000) Accumulation of PAL transcript and PAL activity as affected by heat-conditioning and low-temperature storage and its relation to chilling sensitivity in mandarin fruits. J Agric Food Chem 48:2726–2731

    Article  CAS  PubMed  Google Scholar 

  • Sewell MM, Davis MF, Tuskan GA, Wheeler NC, Elam CC, Bassoni DL, Neale DB (2002) Identification of QTLs influencing wood property traits in loblolly pine (Pinus taeda L.) II. Chemical wood properties. Theor Appl Genet 104:214–222

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327–334

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Wang Z, Bo W, Ren Y, Zhang Z, Zhang D (2012) Transcriptional profiling by cDNA-AFLP analysis showed differential transcript abundance in response to water stress in Populus hopeiensis. BMC Genom 13:286. doi:10.1186/1471-2164-13-286

    Article  CAS  Google Scholar 

  • Song Y, Chen Q, Ci D, Shao X, Zhang D (2014) Effects of high temperature on photosynthesis and related gene expression in poplar. BMC Plant Biol 14:111. doi:10.1186/1471-2229-14-111

    Article  PubMed Central  PubMed  Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc B 64:479–498

    Article  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100:9440–9445

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Triezenberg SJ, Thomashow MF, Stockinger EJ (2005) Multiple hydrophobic motifs in Arabidopsis CBF1 COOH-terminus provide functional redundancy in trans-activation. Plant Mol Biol 58:543–559

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Guan Y, Wu Y, Chen H, Chen F, Chu C (2008) Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol Biol 67:589–602

    Article  CAS  PubMed  Google Scholar 

  • Wei Z, Du Q, Zhang J, Li B, Zhang D (2013) Genetic diversity and population structure in Chinese indigenous poplar (Populus simonii) populations using microsatellite markers. Plant Mol Biol Rep 31:620–632

    Article  CAS  Google Scholar 

  • Xiao H, Tattersall EA, Siddiqua MK, Cramer GR, Nassuth A (2008) CBF4 is a unique member of the CBF transcription factor family of Vitis vinifera and Vitis riparia. Plant Cell Environ 31:1–10

    CAS  PubMed  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (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 ZL, Zhai WJ (2003) Plant physiology laboratory instruction. Higher Education Press, Beijing

    Google Scholar 

  • Zhang ZY, Lin SZ, Zhang Q (2002) Status and advances of molecular genetic improvement of poplar species in China. For Stud China 4:1–8

    Google Scholar 

  • Zhang DQ, Du QZ, Xu BH, Zhang ZY, Li BL (2010) The actin multigene family in Populus: organization, expression and phylogenetic analysis. Mol Genet Genomics 284:105–119

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4:401–406

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from: the Forestry Public Benefit Research Program (No. 201204306), the Specialized Research Fund for the Doctoral Program of Higher Education (No. 20110014110011), and the 111 Project (No. B13007).

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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

    Ying Li, Baohua Xu, Qingzhang Du & Deqiang Zhang

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

    Ying Li, Baohua Xu, Qingzhang Du & Deqiang Zhang

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  1. Ying Li
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Correspondence to Deqiang Zhang.

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Li, Y., Xu, B., Du, Q. et al. Transcript abundance patterns of Populus C-repeat binding factor2 orthologs and genetic association of PsCBF2 allelic variation with physiological and biochemical traits in response to abiotic stress. Planta 242, 295–312 (2015). https://doi.org/10.1007/s00425-015-2307-3

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