SpringerLink
Log in

Characterization of VvPAL-like promoter from grapevine using transgenic tobacco plants

  • Original Article
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

A 2000-bp 5′-flanking region of VvPAL-like was isolated from ‘Summer Black’ grapevine by PCR amplification, named pVvPAL-like. To gain a better understanding of the expression and regulatory mechanism of VvPAL-like, a chimeric expression unit consisting of the β-glucuronidase (GUS) reporter gene under the control of a 2000-bp fragment of the VvPAL-like promoter was transformed into tobacco via Agrobacterium tumefaciens. Histochemical staining showed that the full-length promoter directs efficient expression of the reporter gene in cotyledons and hypocotyls, stigma, style, anthers, pollen, ovary, trichomes, and vascular bundles of transgenic plants. A series of 5′ progressive deletions of the promoter revealed the presence of a negative regulatory region (−424 to −292) in the VvPAL-like promoter. Exposure of the transgenic tobacco plants to various abiotic stresses demonstrated that the full-length construct could be induced by light, copper (Cu), abscisic acid (ABA), indole-3-acetic (IAA), methyl jasmonate (MeJA) (N-1-naphthylphthalamic acid), ethylene, and drought. Furthermore, the ethylene-responsive region was found to be located in the −1461/−930 fragment, while the element(s) for the MeJA-responsive expression may be present in the −424/−292 region in the VvPAL-like promoter. These findings will help us to better understand the molecular mechanisms by which VvPAL-like participates in biosynthesis of flavonoids and stress responses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

Abbreviations

TIBA:

2,3,5-Triiodobenzoic acid

2,4-D:

2,4-Dichlorophenoxya-cetic acid

MU:

4-Methylumbelliferone

MUG:

4-Methylumbelliferyl glucuronide

X-Gluc:

5-Bromo-4-chloro-3-indyle-β-d-glucuronide

ABA:

Abscisic acid

ARFAT:

Auxin response element

BG:

Big green berries

BSA:

Bovine serum albumin

CTAB:

Cetyltriethylammnonium bromide,

FR:

Full red berries

Genoscope:

Grape Genome Browser

HR:

Harvesting red berries

IAA:

Indole-3-acetic

IBA:

Indole-3-butyric acid

IR:

Initial red berries

IPA:

Isopentenyladenosine

MRE:

Metal response element

MeJA:

Methyl jasmonate

NPA:

N-1-naphthylphthalamic acid

NAA:

1-Naphthaleneacetic acid

NCBI:

National Center for Biotechnology Information

PR:

Partial red berries

PAL :

Phenylalanine ammonia-lyase

qRT-PCR:

Quantitative real-time polymerase chain reaction

SA:

Salicylic acid

SG:

Small green berries

TSS:

Transcriptional start sites

T-DNA:

Transfer DNA

GUS:

β-Glucuronidase gene

References

  • Aloni R (1987) Differentiation of vascular tissues. Annu Rev Plant Physiol 38:179–204

    Article  Google Scholar 

  • An G, Kim Y, Glick BR, Thompson JE (1993) Techniques for isolating and characterizing plant transcription promoters, enhancers, and terminators. Methods in plant molecular biology and biotechnology., pp 155–166

    Google Scholar 

  • Boter M, Ruíz-Rivero O, Abdeen A, Prat S (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Gene Dev 18:1577–1591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Burrow D, Chlan CA, Sen P, Murai N (1990) High frequency generation of transgenic tobacco plants after modified leaf disk cocultivation with Agrobacterium tumefaciens. Plant Mol Biol Rep 8:124–139

    Article  Google Scholar 

  • Campbell MM, Ellis BE (1992) Fungal elicitor-mediated responses in pine cell cultures: III. Purification and characterization of phenylalanine ammonia-lyase. Plant Physiol 98:62–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collinge DB, Slusarenko AJ (1987) Plant gene expression in response to pathogens. Plant Mol Biol 9:389–410

    Article  CAS  PubMed  Google Scholar 

  • Cramer CL et al (1985) Co-ordinated synthesis of phytoalexin biosynthetic enzymes in biologically-stressed cells of bean (Phaseolus vulgaris L.). EMBO J 4:285–289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cramer CL et al (1989) Phenylalanine ammonia-lyase gene organization and structure. Plant Mol Biol 12:367–383

    Article  CAS  PubMed  Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon RA, Steele CL (1999) Flavonoids and isoflavonoidsa gold mine for metabolic engineering. Trends Plant Sci 4:394–400

    Article  PubMed  Google Scholar 

  • Dong X, Mindrinos M, Davis K, Ausubel F (1991) Induction of Arabidopsis defense genes by virulent and avirutent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 3:61–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards K, Cramer CL, Bolwell GP, Dixon RA, Schuch W, Lamb CJ (1985) Rapid transient induction of phenylalanine ammonia-lyase mRNA in elicitor-treated bean cells. Proc Natl Acad Sci 82:6731–6735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frank RL, Vodkin LO (1991) Sequence and structure of a phenylalanine ammonia-lyase gene from Glycine max. J DNA Seq Mapp 1:335–346

    Article  CAS  Google Scholar 

  • Gao ZM, Wang XC, Peng ZH, Zheng B, Liu Q (2012) Characterization and primary functional analysis of phenylalanine ammonia-lyase gene from Phyllostachys edulis. Plant Cell Rep 31:1345–1356

    Article  CAS  PubMed  Google Scholar 

  • Glover BJ (2000) Differentiation in plant epidermal cells. J Exp Bot 51:497–505

    Article  CAS  PubMed  Google Scholar 

  • Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 134:1555–1573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gowri G, Paiva NL, Dixon RA (1991) Stress responses in alfalfa (Medicago sativa L.)12. Sequence analysis of phenylalanine ammonia-lyase (PAL) cDNA clones and appearance of PAL transcripts in elicitor-treated cell cultures and develo** plants. Plant Mol Biol 17:415–429

    Article  CAS  PubMed  Google Scholar 

  • Gray-Mitsumune M, Molitor EK, Cukovic D, Carlson JE, Douglas CJ (1999) Developmentally regulated patterns of expression directed by poplar PAL promoters in transgenic tobacco and poplar. Plant Mol Biol 39:657–669

    Article  CAS  PubMed  Google Scholar 

  • Harborne JB (1993) The flavonoids: advances in research since 1986. Chapman & Hall, London, pp 449–564

    Google Scholar 

  • Harborne JB, Grayer RJ (1994) Flavonoids and insects. In: Harborne JB (ed) The flavonoids: advances in research since 1986. Chapman & Hall, London, pp 589–618

    Chapter  Google Scholar 

  • Heath IB (1990) Tip growth in plant and fungal cells. Academic Press, New York, pp 1–351

    Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holton T, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7:1071–1083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SA, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1229–1230

    Article  CAS  Google Scholar 

  • Hsu C, Roy GC, Jenkins JN, Ma D (1999) Analysis of promoter activity of cotton lipid transfer protein gene LTP6 in transgenic tobacco plants. Plant Sci 143:63–70

    Article  CAS  Google Scholar 

  • Jain S, Kumar D, Jain M, Chaudhary P, Deswal R, Sarin NB (2012) Ectopic overexpression of a salt stress-induced pathogenesis-related class 10 protein (PR10) gene from peanut (Arachis hypogaea L.) affords broad spectrum abiotic stress tolerance in transgenic tobacco. Plant Cell Tiss Organ Cult 109:19–31

    Article  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jia H et al (2015) Jasmonic acid involves in grape fruit ripening and resistant against botrytis cinerea. Funct Integr Genomics 16(1):1–16

    Google Scholar 

  • Jots HJ, Hahlbrock K (1992) Phenylalanine ammonia-lyase in potato (Solanum tuberosum L.). Genomic complexity, structural comparison of two selected genes and modes of expression. Eur J Biochem 204:621–629

    Article  Google Scholar 

  • Kawamata S et al (1992) Molecular cloning of phenylalanine ammonia-lyase cDNA from Pisum sativum. Plant Mol Biol 20:167–170

    Article  CAS  PubMed  Google Scholar 

  • Keith RD (1991) Virulence of selected phytopathogenic pseudomonads in Arabidopsis thaliana. Mol Plant-Microbe Interact 4:477–788

    Article  Google Scholar 

  • Kervinen T, Peltonen S, Utriainen M, Kangasjärvi J, Teeri TH, Karjalainen R (1997) Cloning and characterization of cDNA clones encoding phenylalanine ammonia-lyase in barley. Plant Sci 123:143–150

    Article  CAS  Google Scholar 

  • Kim HJ, Triplett BA (2001) Cotton fiber growth in planta and in vitro: models for plant cell elongation and cell wall biogenesis. Plant Physiol 127:1361–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiran K et al (2006) The TATA-box sequence in the basal promoter contributes to determining light-dependent gene expression in plants. Plant Physiol 142:364–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuhn DN, Chappell J, Boudet A, Hahlbrock K (1984) Induction of phenylalanine ammonia-lyase and 4-coumarate: CoA ligase mRNAs in cultured plant cells by UV light or fungal elicitors. Proc Natl Acad Sci 81:1102–1106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lawton MA, Dixon RA, Hahlbrock K, Lamb C (1983) Rapid induction of the synthesis of phenylalanine ammonia-lyase and of chalcone synthase in elicitor-treated plant cells. Eur J Biochem 129:593–601

    Article  CAS  PubMed  Google Scholar 

  • Lee SW, Robb J, Nazar RN (1992) Truncated phenylalanine ammonia-lyase expression in tomato (Lycopersicon esculentum). J Biol Chem 267:11824–11830

    CAS  PubMed  Google Scholar 

  • Lescot M et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang X, Dron M, Cramer CL, Dixon RA, Lamb CJ (1989a) Differential regulation of phenylalanine ammonia-lyase genes during plant development and by environmental cues. J Biol Chem 264:14486–14492

    CAS  PubMed  Google Scholar 

  • Liang XW, Dron M, Schmid J, Dixon RA, Lamb CJ (1989b) Development and environmental regulation of a phenylalanine ammonia-lyase-beta-glucuronidase gene fusion in transgenic tobacco plants. Proc Natl Acad Sci 86:9284–9288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu HC, Creech RG, Jenkins JN, Ma DP (2000) Cloning and promoter analysis of the cotton lipid transfer protein gene Ltp3. Biochim Biophys Acta 1487:106–111

    Article  CAS  PubMed  Google Scholar 

  • Lois R, Hahlbrock K (1992) Differential wound activation of members of the phenylalanine ammonia-lyase and 4-coumarate-CoA ligase gene families in various organs of parsley plants. Z Naturforsch C 47:90–94

    CAS  PubMed  Google Scholar 

  • Lois R, Dietrich A, Hahlbrock K, Schulz WA (1989) Phenylalanine ammonia-lyase gene from parsley: structure, regulation and identification of elicitor and light responsive cis-acting elements. EMBO J 8:1641–1648

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lomax TL, Muday GK, Rubery PH (1995) Auxin transport. In: Davies PJ (ed) Plant hormones: physiology, biochemistry and molecular biology. Kluwer, Dordrecht, pp 509–530

    Chapter  Google Scholar 

  • Lu BB et al (2006) Cloning and characterization of a differentially expressed phenylalanine ammonia-lyase gene (IiPAL) after genome duplication from tetraploid Isatis indigotica Fort. J Integr Plant Biol 48:1439–1449

    Article  CAS  Google Scholar 

  • Meisel LA, Lam E (1996) The conserved ELK-homeodomain of KNOTTED-1 contains two regions that signal nuclear localization. Plant Mol Biol 30:1–14

    Article  CAS  PubMed  Google Scholar 

  • Minami E, Tanaka Y (1993) Nucleotide sequence of the gene for phenylalanine ammonia lyase of rice and its deduced amino acid sequence. Biochem Biophys Acta 1171:321–322

    CAS  PubMed  Google Scholar 

  • Minami E, Ozeki Y, Matsuoka M, Koizuka N, Tanaka Y (1989) Structure and some characterization of the gene for phenylalanine ammonia-lyase from rice plants. Eur J Biochem 185:19–25

    Article  CAS  PubMed  Google Scholar 

  • Ohl S, Hedrick SA, Chory J, Lamb CJ (1990) Functional properties of a phenylalanine ammonia-lyase promoter from Arabidopsis. Plant Cell 2:837–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oppenheimer DG, Herman PL, Sivakumaran S, Esch J, Marks MD (1990) A MYB gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67:483–493

    Article  Google Scholar 

  • Osakabe Y, Osakabe K, Chiang VL (2009) Characterization of the tissue-specific expression of phenylalanine ammonia-lyase gene promoter from loblolly pine (Pinus taeda) in Nicotiana tabacum. Plant Cell Rep 28:1309–1317

    Article  CAS  PubMed  Google Scholar 

  • Sachs T (1991) Cell polarity and tissue patterning in plants. Development 78:83–93

    Google Scholar 

  • Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Schmidt K, Heberle B, Kurrasch J, Nehls R, Stahl DJ (2004) Suppression of phenylalanine ammonia-lyase expression in sugar beet by the fungal pathogen Cercospora beticola is mediated at the core promoter of the gene. Plant Mol Biol 55:835–852

    Article  CAS  PubMed  Google Scholar 

  • Shangguan XX, Xu B, Yu ZX, Wang LJ, Chen XY (2008) Promoter of a cotton fibre MYB gene functional in trichomes of Arabidopsis and glandular trichomes of tobacco. J Exp Bot 59:3533–3542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shufflebottom D, Edwards K, Sehneh W, Bevan M (1993) Transcription of two members of a gent family encoding phenylalanine ammonia-lyase leads to remarkably different cell specificities and induction patterns. Plant J 3:835–845

    Article  CAS  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 94:1035–1040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Subramaniam R, Reinold S, Molitor EK, Douglas CJ (1993) Structure, inheritance, and expression of hybrid poplar (Populus trichocarpa × Populus deltoides) phenylalanine ammonia-lyase genes. Plant Physiol 102:71–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka Y, Matsuoka M, Yamanoto N, Ohashi Y, Kano-Murakami Y, Ozeki Y (1989) Structure and characterization of a cDNA clone for phenylalanine ammonia-lyase from cut-injured roots of sweet potato. Plant Physiol 90:1403–1407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walker-peach CR, Velten J (1994) Agrobacterium-mediated gene transfer to plant cells: cointegrate and binary vector systems. In Plant molecular biology manual. Springer, Netherlands, pp 33–51

    Google Scholar 

  • Wang L, An C, Qian W, Liu T, Li J, Chen Z (2004a) Detection of the putative cis-region involved in the induction by a Pyricularia oryzae elicitor of the promoter of a gene encoding phenylalanine ammonia-lyase in rice. Plant Cell Rep 22:513–518

    Article  CAS  PubMed  Google Scholar 

  • Wang S et al (2004b) Control of plant trichome development by a cotton fiber MYB gene. Plant Cell 16(9):2323–2334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XD, Wang ZP, Zou YP (1996) Improved procedure for the isolation of nuclear DNA from leaves of wild grapevine dried with silica gel. Plant Mol Biol Rep 14:369–373

    Article  CAS  Google Scholar 

  • Wanner LA, Li G, Ware D, Somssich IE, Davis KR (1995) The phenylalanine ammonia-lyase gene family in Arabidopsis thaliana. Plant Mol Biol 27:327–338

    Article  CAS  PubMed  Google Scholar 

  • Wanner LA, Mittal S, Davis KR (1993) Recognition of the avirulence gene avrB from Pseudomonas syringae pv. glycinea by Arabidopsis thaliana. Mol Plant Microbe Interact 6:582–591

    Article  CAS  PubMed  Google Scholar 

  • Whetten RW, Sederoff RR (1992) Phenylalanine ammonia-lyase from loblolly pine: purification of the enzyme and isolation of complementary DNA clones. Plant Physiol 98:380–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong JH, Namasivayam P, Abdullah MP (2012) The PAL2 promoter activities in relation to structural development and adaptation in Arabidopsis thaliana. Planta 235:267–277

    Article  CAS  PubMed  Google Scholar 

  • Wu AM, Lv SY, Liu JY (2007) Functional analysis of a cotton glucuronosyltransferase promoter in transgenic tobaccos. Cell Res 17:174–183

    Article  CAS  PubMed  Google Scholar 

  • Xu F, Cai R, Cheng S, Du H, Wang Y, Cheng S (2008) Molecular cloning, characterization and expression of phenylalanine ammonia-lyase gene from Ginkgo biloba. Afr J Biotechnol 7:721–729

    Google Scholar 

  • Yamada T et al (1992) Phenylalanine ammonia-lyase genes from Pisum sativum: structure, organ-specific expression and regulation by fungal elicitor and suppressor. Plant Cell Physiol 33:715–725

    CAS  Google Scholar 

Download references

Acknowledgments

The study was funded by the Important National Science & Technology Specific Projects (No. 2012FY110100-3) and the Fundamental Research Funds for the Central Universities of China (KYZ201411). We thank all laboratory members for help, advice, and discussion.

Author information

Authors and Affiliations

  1. Key Laboratory of Genetics and Fruit development, College of Horticulture, Nan**g Agricultural University, Nan**g city, Jiangsu Province, People’s Republic of China

    SongTao Jiu, Chen Wang, Ting Zheng, Zhongjie Liu, **angPeng Leng, Tariq Pervaiz & **gGui Fang

  2. Department of Plant Molecular Biotechnology, Institute of Agricultural Biotechnology, National Institute of Genetic Engineering and Biotechnology (NIGEB), Tehran, Iran

    Abolfazl Lotfi

  3. Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nan**g city, Jiangsu Province, People’s Republic of China

    **aoMin Wang

Authors
  1. SongTao Jiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ting Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhongjie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. **angPeng Leng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tariq Pervaiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Abolfazl Lotfi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. **gGui Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. **aoMin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to **gGui Fang or **aoMin Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests. All authors have read and approved the final manuscript.

Electronic Supplementary Materials

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

Multiple alignment of the amino acid sequences of VvPAL-like and nine plant PALs preformed in DNAMAN. The conserved nucleotides are shaded. The PALs included in the alignment were from Arabidopsis thaliana (Gene ID: 19310726), Oryza sativa (Gene ID: 4330040), Zea mays (Gene ID: 100127011), Glycine max (Gene ID: 100787872), Fragaria vesca (Gene ID: 101315259), Solanum lycopersicum (Gene ID: 101261892), Cucumis sativus (Gene ID: 101218856), Cucumis melo (Gene ID: 103501962), and Malus domestica (Gene ID: 103450046), respectively. (TIF 56971 kb)

Supplementary Fig. 2

Phylogenetic tree of PAL genes from different species. The tree was constructed by the neighbor-joining method. The Bootstrap consensus tree was constructed based on a multiple alignment of PAL genes from Arabidopsis thaliana, Oryza sativa, Zea mays, Glycine max, Fragaria vesca, Solanum lycopersicum, Cucumis sativus, Cucumis melo, Malus domestica and Vitis vinifera. Bootstrap values (in percentage) are shown at branch nodes. (PDF 7 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiu, S., Wang, C., Zheng, T. et al. Characterization of VvPAL-like promoter from grapevine using transgenic tobacco plants. Funct Integr Genomics 16, 595–617 (2016). https://doi.org/10.1007/s10142-016-0516-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-016-0516-x

Keywords

Search

Navigation