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Transcriptome dynamics of a desert poplar (Populus pruinosa) in response to continuous salinity stress

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Abstract

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Using RNA sequencing analysis, we identified 9,216 regulatory and salt-related genes with differential expression and temporal expression trends which provide a clear picture of transcriptomic dynamics in response to continuous salinity stress in a desert poplar, Populus pruinosa.

Abstract

Populus pruinosa Schrenk is native to the desert region of western China and extraordinarily well adapted to the local salt stress. Thus, it is an ideal model for studying plants’ adaptation to salt stress, but its transcriptomic responses have not been previously characterized. Thus, we analyzed time- courses of these responses via a series of sequencings. In total, we generated 157.4 million 100 bp paired-end clean reads and identified 9,216 differentially expressed genes (DEGs) between salt-stressed calli and controls. Gene ontology classification analysis revealed that salt stress-related categories––including ‘oxidation reduction’, ‘transcription factor activity’, ‘membrane’ and ‘ion channel activity’––were highly enriched among these DEGs. In addition, we grouped the 9,216 DEGs by their expression dynamics into four clusters, and the genes in each cluster showed enrichment for particular functional categories. We also found that most DEGs were activated within 24 h of the stress and their expression stabilized after 48 h. All these findings suggest that gene expression rapidly and coordinately changes during this species’ adaptation to salt stress. In addition, the identified DEGs provide critical genetic resources for further functional analyses and indications of potential transgenic modifications for developing salt-tolerant poplars.

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Abbreviations

DEG:

Differentially expressed gene

FPKM:

Number of fragments per kilobase of exon per million fragments mapped

FDR:

False discovery rate

RNA-Seq:

High throughput sequencing of cDNA libraries

cDNA:

Complementary DNA synthesized from RNA

CDS:

Coding DNA sequences

qRT-PCR:

Quantitative real-time polymerase chain reaction

GO:

Gene ontology

KEGG:

Kyoto encyclopedia of genes and genomes

Nr:

Non-redundant database

COG:

Cluster of orthologous groups databases

References

  • Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol 123:1047–1056

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Arbona V, Manzi M, Ollas C, Gomez-Cadenas A (2013) Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int J Mol Sci 14:4885–4911

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    Article  CAS  Google Scholar 

  • Beritognolo I, Harfouche A, Brilli F, Prosperini G, Gaudet M, Brosche M, Salani F, Kuzminsky E, Auvinen P, Paulin L, Kangasjarvi J, Loreto F, Valentini R, Mugnozza GS, Sabatti M (2011) Comparative study of transcriptional and physiological responses to salinity stress in two contrasting Populus alba L. genotypes. Tree Physiol 31:1335–1355

    Article  CAS  PubMed  Google Scholar 

  • Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta 1465:140–151

    Article  CAS  PubMed  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  • Brinker M, Brosche M, Vinocur B, Abo-Ogiala A, Fayyaz P, Janz D, Ottow EA, Cullmann AD, Saborowski J, Kangasjarvi J, Altman A, Polle A (2010) Linking the salt transcriptome with physiological responses of a salt-resistant Populus species as a strategy to identify genes important for stress acclimation. Plant Physiol 154:1697–1709

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bullard J, Purdom E, Hansen K, Dudoit S (2010) Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinform 11:94

    Article  Google Scholar 

  • Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, Nawrocki EP, Eddy SR, Gardner PP, Bateman A (2013) Rfam 11.0: 10 years of RNA families. Nucleic Acids Res 41:D226–D232

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Chen S, Li J, Fritz E, Wang S, Hüttermann A (2002) Sodium and chloride distribution in roots and transport in three poplar genotypes under increasing NaCl stress. For Ecol Manage 168:217–230

    Article  Google Scholar 

  • Chen S, Jiang J, Li H, Liu G (2012) The salt-responsive transcriptome of Populus simonii × Populus nigra via DGE. Gene 504:203–212

    Article  CAS  PubMed  Google Scholar 

  • Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795–803

    Article  CAS  Google Scholar 

  • Conde A, Chaves MM, Gerós H (2011) Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol 52:1583–1602

    CAS  PubMed  Google Scholar 

  • Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Eckenwalder JE (1996) Systematics and evolution of Populus. In: Stettler RF, Heilman JPE, Hinckley TM (eds) In biology of populus. NRC Research, Ottawa, pp 7–32

    Google Scholar 

  • Forrest K, Bhave M (2007) Major intrinsic proteins (MIPs) in plants: a complex gene family with major impacts on plant phenotype. Funct Integr Genomics 7:263–289

    Article  CAS  PubMed  Google Scholar 

  • Frith MC, Fu Y, Yu L, Chen JF, Hansen U, Weng Z (2004) Detection of functional DNA motifs via statistical over-representation. Nucleic Acids Res 32:1372–1381

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, Macmanes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, Leduc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    CAS  PubMed  Google Scholar 

  • Hukin D, Cochard H, Dreyer E, Thiec DL, Bogeat-Triboulot MB (2005) Cavitation vulnerability in roots and shoots: does Populus euphratica Oliv., a poplar from arid areas of Central Asia, differ from other poplar species? J Exp Bot 56:2003–2010

    Article  CAS  PubMed  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    CAS  PubMed  Google Scholar 

  • Janz D, Behnke K, Schnitzler J-P, Kanawati B, Schmitt-Kopplin P, Polle A (2010) Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms. BMC Plant Biol 10:150

    Article  PubMed Central  PubMed  Google Scholar 

  • Jiang Z, Liu X, Peng Z, Wan Y, Ji Y, He W, Wan W, Luo J, Guo H (2011) AHD2.0: an update version of Arabidopsis Hormone Database for plant systematic studies. Nucleic Acids Res 39:D1123–D1129

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg S (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  PubMed Central  PubMed  Google Scholar 

  • Langridge P, Paltridge N, Fincher G (2006) Functional genomics of abiotic stress tolerance in cereals. Brief Funct Genomic Proteomic 4:343–354

    Article  CAS  PubMed  Google Scholar 

  • Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659

    Article  CAS  PubMed  Google Scholar 

  • Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR, Reidel EJ, Turgeon R, Liu P, Sun Q, Nelson T, Brutnell TP (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42:1060–1067

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma HC, Fung L, Wang SS, Altman A, Hüttermann A (1997) Photosynthetic response of Populus euphratica to salt stress. For Ecol Manage 93:55–61

    Article  Google Scholar 

  • Ma Q, Dai X, Xu Y, Guo J, Liu Y, Chen N, Xiao J, Zhang D, Xu Z, Zhang X, Chong K (2009) Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and Ectopic expression of stress genes. Plant Physiol 150:244–256

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ma T, Wang J, Zhou G, Yue Z, Hu Q, Chen Y, Liu B, Qiu Q, Wang Z, Zhang J, Wang K, Jiang D, Gou C, Yu L, Zhan D, Zhou R, Luo W, Ma H, Yang Y, Pan S, Fang D, Luo Y, Wang X, Wang G, Wang J, Wang Q, Lu X, Chen Z, Liu J, Lu Y, Yin Y, Yang H, Abbott RJ, Wu Y, Wan D, Li J, Yin T, Lascoux M, Difazio SP, Tuskan GA, Wang J, Jianquan L (2013) Genomic insights into salt adaptation in a desert poplar. Nat Commun 4:2797

    PubMed  Google Scholar 

  • Meiri D, Breiman A (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J 59:387–399

    Article  CAS  PubMed  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Ottow EA, Brinker M, Teichmann T, Fritz E, Kaiser W, Brosche M, Kangasjarvi J, Jiang X, Polle A (2005) Populus euphratica displays apoplastic sodium accumulation, osmotic adjustment by decreases in calcium and soluble carbohydrates, and develops leaf succulence under salt stress. Plant Physiol 139:1762–1772

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Qiu Q, Ma T, Hu Q, Liu B, Wu Y, Zhou H, Wang Q, Wang J, Liu J (2011) Genome-scale transcriptome analysis of the desert poplar, Populus euphratica. Tree Physiol 31:452–461

    Article  PubMed  Google Scholar 

  • Ren Q, Kang KH, Paulsen IT (2004) TransportDB: a relational database of cellular membrane transport systems. Nucleic Acids Res 32:D284–D288

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rus AM, Bressan RA, Hasegawa PM (2005) Unraveling salt tolerance in crops. Nat Genet 37(10):1029–1030

    Article  CAS  PubMed  Google Scholar 

  • Sandelin A, Alkema W, Engström P, Wasserman WW, Lenhard B (2004) JASPAR: an open-access database for eukaryotic transcription factor binding profiles. Nucleic Acids Res 32:D91–D94

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1,300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61–72

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7,000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    Article  CAS  PubMed  Google Scholar 

  • Selote DS, Khanna-Chopra R (2006) Drought acclimation confers oxidative stress tolerance by inducing co-ordinated antioxidant defense at cellular and subcellular level in leaves of wheat seedlings. Physiol Plant 127:494–506

    Article  CAS  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 

  • Sun J, Chen S, Dai S, Wang R, Li N, Shen X, Zhou X, Lu C, Zheng X, Hu Z, Zhang Z, Song J, Xu Y (2009) NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species. Plant Physiol 149:1141–1153

    Article  CAS  PubMed Central  PubMed  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 G-L, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin 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, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé J-C, 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, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai C-J, 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  CAS  PubMed  Google Scholar 

  • Tuteja N (2007) Mechanisms of high salinity tolerance in plants. In: Dieter H, Helmut S (eds) Methods in enzymology, vol 428. Academic, USA, pp 419–438

    Google Scholar 

  • Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25(2):173–194

    Article  CAS  PubMed  Google Scholar 

  • Uchiyama I, Higuchi T, Kawai M (2010) MBGD update 2010: toward a comprehensive resource for exploring microbial genome diversity. Nucleic Acids Res 38:D361–D365

    Article  CAS  PubMed Central  PubMed  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 

  • Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456:470–476

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang J, Wu Y, Ren G, Guo Q, Liu J, Lascoux M (2011) Genetic differentiation and delimitation between ecologically diverged Populus euphratica and P. pruinosa. PLoS One 6:e26530

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xu Z-S, Xia L-Q, Chen M, Cheng X-G, Zhang R-Y, Li L-C, Zhao Y-X, Lu Y, Ni Z-Y, Liu L, Qiu Z-G, Ma Y-Z (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 65:719–732

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ye C-Y, Zhang H-C, Chen J-H, Xia X-L, Yin W-L (2009) Molecular characterization of putative vacuolar NHX-type Na+/H+ exchanger genes from the salt-resistant tree Populus euphratica. Physiol Plant 137:166–174

    Article  CAS  PubMed  Google Scholar 

  • Yeo A (1998) Predicting the interaction between the effects of salinity and climate change on crop plants. Sci Hortic 78:159–174

    Article  Google Scholar 

  • Yeung KY, Haynor DR, Ruzzo WL (2001) Validating clustering for gene expression data. Bioinformatics 17:309–318

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Jin J, Tang L, Zhao Y, Gu X, Gao G, Luo J (2011) PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 39:D1114–D1117

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang J, Xie P, Lascoux M, Meagher TR, Liu J (2013) Rapidly evolving genes and stress adaptation of two desert poplars, Populus euphratica and P. pruinosa. PLoS One 8:e66370

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu J-K (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  PubMed  Google Scholar 

  • Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ziemann M, Kamboj A, Hove RM, Loveridge S, El-Osta A, Bhave M (2013) Analysis of the barley leaf transcriptome under salinity stress using mRNA-Seq. Acta Physiologiae Plantarum 35:1915–1924

    Article  CAS  Google Scholar 

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Acknowledgments

Financial support was provided by the National High-Tech Research and Development Program of China (863 Program, No. 2013AA102605), the National Science Foundation of China (30972336, 31270652) and the Xinjiang Production and Construction Corps Key Laboratory of Protection and Utilization of Biological Resources in Tarim Basin opening topic fund (BRZD1204). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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The authors declare that they have no conflict of interest.

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Correspondence to Dongshi Wan.

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Communicated by Manoj Prasad.

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Zhang, J., Jiang, D., Liu, B. et al. Transcriptome dynamics of a desert poplar (Populus pruinosa) in response to continuous salinity stress. Plant Cell Rep 33, 1565–1579 (2014). https://doi.org/10.1007/s00299-014-1638-z

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