Plant Molecular Biology

, Volume 82, Issue 4–5, pp 393–416 | Cite as

Characterization of the GGPP synthase gene family in Arabidopsis thaliana

  • Gilles Beck
  • Diana Coman
  • Edgar Herren
  • M. Águila Ruiz-Sola
  • Manuel Rodríguez-Concepción
  • Wilhelm Gruissem
  • Eva Vranová
Article

Abstract

Geranylgeranyl diphosphate (GGPP) is a key precursor of various isoprenoids that have diverse functions in plant metabolism and development. The annotation of the Arabidopsis thaliana genome predicts 12 genes to encode geranylgeranyl diphosphate synthases (GGPPS). In this study we analyzed GGPPS activity as well as the subcellular localization and tissue-specific expression of the entire protein family in A. thaliana. GGPPS2 (At2g18620), GGPPS3 (At2g18640), GGPPS6 (At3g14530), GGPPS7 (At3g14550), GGPPS8 (At3g20160), GGPPS9 (At3g29430), GGPPS10 (At3g32040) and GGPPS11 (At4g36810) showed GGPPS activity in Escherichia coli, similar to activities reported earlier for GGPPS1 (At1g49530) and GGPPS4 (At2g23800) (Zhu et al. in Plant Cell Physiol 38(3):357–361, 1997a; Plant Mol Biol 35(3):331–341, b). GGPPS12 (At4g38460) did not produce GGPP in E. coli. Based on DNA sequence analysis we propose that GGPPS5 (At3g14510) is a pseudogene. GGPPS–GFP (green fluorescent protein) fusion proteins of the ten functional GGPP synthases localized to plastids, mitochondria and the endoplasmic reticulum, with the majority of the enzymes located in plastids. Gene expression analysis using quantitative real time-PCR, GGPPS promoter-GUS (β-glucuronidase) assays and publicly available microarray data revealed a differential spatio-temporal expression of GGPPS genes. The results suggest that plastids and mitochondria are key subcellular compartments for the synthesis of ubiquitous GGPP-derived isoprenoid species. GGPPS11 and GGPPS1 are the major isozymes responsible for their biosynthesis. All remaining paralogs, encoding six plastidial isozymes and two cytosolic isozymes, were expressed in specific tissues and/or at specific developmental stages, suggesting their role in developmentally regulated isoprenoid biosynthesis. Our results show that of the 12 predicted GGPPS encoded in the A. thaliana genome 10 are functional proteins that can synthesize GGPP. Their specific subcellular location and differential expression pattern suggest subfunctionalization in providing GGPP to specific tissues, developmental stages, or metabolic pathways.

Keywords

Arabidopsis Isoprenoids Branchpoint Prenyl diphosphate synthase Geranylgeranyl diphosphate synthase 

Abbreviations

ABA

Abscisic acid

DMAPP

Dimethylallyl diphosphate

ER

Endoplasmic reticulum

FPP

Farnesyl diphosphate

GA

Gibberellic acid

GFP

Green fluorescent protein

GGPP

Geranylgeranyl diphosphate

GGPPS

Geranylgeranyl diphosphate synthase

GPP

Geranyl diphosphate

GUS

β-Glucuronidase

IPP

Isopentenyl diphosphate

MEP

Methylerythritol

MVA

Mevalonate

Notes

Acknowledgments

This work was supported by a grant from ETH Zurich (TH-51 06-1) and the EU FP7 contract 245143 (TiMet). The Spanish Ministerio de Ciencia e Innovacion (www.micinn.es) provided grants BIO2008-00432 and BIO2011-23680 to MRC and a doctoral FPI fellowship to ARS. We thank Biswapriya Biswavas Misra and Christian Barucker for their contribution to the work on subcellular localization. We thank Dr. Axel Schmidt for useful discussions on enzymatic activity assays.

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

11103_2013_70_MOESM1_ESM.pdf (232 kb)
Supplemental Table S1 as PDF Oligonucleotides used for GGPPSs amplification to construct pGEX-GGPPS (PDF 231 kb)
11103_2013_70_MOESM2_ESM.pdf (236 kb)
Supplemental Table S2 as PDF Oligonucleotides used for GGPPSs amplification to construct pENTR/D-TOPO-GGPPS-3` (PDF 235 kb)
11103_2013_70_MOESM3_ESM.pdf (249 kb)
Supplemental Table S3 as PDF Oligonucleotides used for RT-qPCR (PDF 248 kb)
11103_2013_70_MOESM4_ESM.pdf (35 kb)
Supplemental Table S4 as PDF Oligonucleotides used for GGPPSs promoter amplification to construct pENTR-D-TOPO-GGPPSpro (PDF 34 kb)
11103_2013_70_MOESM5_ESM.pdf (2.6 mb)
Supplemental Table S5 as PDF RT-qPCR and microarray expression of GGPPSs in seven Arabidopsis organs (PDF 2710 kb)
11103_2013_70_MOESM6_ESM.pdf (1.9 mb)
Supplemental Table S6 as PDF Microarray tissue-specific expression of the GGPPS genes (PDF 1986 kb)

References

  1. Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O (2006) The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 16(6):553–563PubMedCrossRefGoogle Scholar
  2. Bick JA, Lange BM (2003) Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arch Biochem Biophys 415(2):146–154PubMedCrossRefGoogle Scholar
  3. Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, Benfey PN (2003) A gene expression map of the Arabidopsis root. Science 302(5652):1956–1960PubMedCrossRefGoogle Scholar
  4. Bouvier F, Suire C, d’Harlingue A, Backhaus RA, Camara B (2000) Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. Plant J 24(2):241–252PubMedCrossRefGoogle Scholar
  5. Caughey WS, Smythe GA, O’Keeffe DH, Maskasky JE, Smith MI (1975) Heme A of cytochrome c oxicase. Structure and properties: comparisons with hemes B, C, and S and derivatives. J Biol Chem 250(19):7602–7622PubMedGoogle Scholar
  6. Closa M, Vranová E, Bortolotti C, Bigler L, Arró M, Ferrer A, Gruissem W (2010) The Arabidopsis thaliana FPP synthase isozymes have overlapping and specific functions in isoprenoid biosynthesis, and complete loss of FPP synthase activity causes early developmental arrest. Plant J 63(3):512–525CrossRefGoogle Scholar
  7. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743PubMedCrossRefGoogle Scholar
  8. Cunillera N, Arró M, Delourme D, Karst F, Boronat A, Ferrer A (1996) Arabidopsis thaliana contains two differentially expressed farnesyl-diphosphate synthase genes. J Biol Chem 271(13):7774–7780PubMedCrossRefGoogle Scholar
  9. Cunillera N, Boronat A, Ferrer A (1997) The Arabidopsis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J Biol Chem 272(24):15381–15388PubMedCrossRefGoogle Scholar
  10. Czechowski T, Bari RP, Stitt M, Scheible W-R, Udvardi MK (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J 38(2):366–379PubMedCrossRefGoogle Scholar
  11. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible W-R (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139(1):5–17PubMedCrossRefGoogle Scholar
  12. Delourme D, Lacroute F, Karst F (1994) Cloning of an Arabidopsis thaliana cDNA coding for farnesyl diphosphate synthase by functional complementation in yeast. Plant Mol Biol 26(6):1867–1873PubMedCrossRefGoogle Scholar
  13. Ducluzeau A-L, Wamboldt Y, Elowsky CG, Mackenzie SA, Schuurink RC, Basset GJC (2011) Gene network reconstruction identifies the authentic trans-prenyl diphosphate synthase that makes the solanesyl moiety of ubiquinone-9 in Arabidopsis. Plant J 69(2):366–375PubMedCrossRefGoogle Scholar
  14. Dugardeyn J, Vandenbussche F, Van Der Straeten D (2008) To grow or not to grow: what can we learn on ethylene-gibberellin cross-talk by in silico gene expression analysis? J Exp Bot 59(1):1–16PubMedCrossRefGoogle Scholar
  15. Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300(4):1005–1016PubMedCrossRefGoogle Scholar
  16. Floss DS, Walter M (2009) Role of carotenoid cleavage dioxygenase 1(CCD1) in apocarotenoid biogenesis revisited. Plant Signaling Behav 4(3):172–175CrossRefGoogle Scholar
  17. Flügge U-I, Gao W (2005) Transport of isoprenoid intermediates across chloroplast envelope membranes. Plant Biol 1:91–97CrossRefGoogle Scholar
  18. Hojo M, Matsumoto T, Miura T (2007) Cloning and expression of a geranylgeranyl diphosphate synthase gene: insights into the synthesis of termite defence secretion. Insect Mol Biol 16(1):121–131PubMedCrossRefGoogle Scholar
  19. Hruz T, Wyss M, Docquier M, Pfaffl M, Masanetz S, Borghi L, Verbrugghe P, Kalaydjieva L, Bleuler S, Laule O, Descombes P, Gruissem W, Zimmermann P (2011) RefGenes: identification of reliable and condition specific reference genes for RT-qPCR data normalization. BMC Genomics 12(1):156PubMedCrossRefGoogle Scholar
  20. Hsieh F-L, Chang T-H, Ko T-P, Wang AH-J (2011) Structure and mechanism of an Arabidopsis medium/long-chain-length prenyl pyrophosphate synthase. Plant Physiol 155(3):1079–1090PubMedCrossRefGoogle Scholar
  21. Hu J, Mitchum MG, Barnaby N, Ayele BT, Ogawa M, Nam E, Lai W-C, Hanada A, Alonso JM, Ecker JR, Swain SM, Yamaguchi S, Kamiya Y, Sun T-p (2008) Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 20(2):320–336PubMedCrossRefGoogle Scholar
  22. Huang M, Abel C, Sohrabi R, Petri J, Haupt I, Cosimano J, Gershenzon J, Tholl D (2010) Variation of herbivore-induced volatile terpenes among Arabidopsis ecotypes depends on allelic differences and subcellular targeting of two terpene synthases, TPS02 and TPS03. Plant Physiol 153(3):1293–1310PubMedCrossRefGoogle Scholar
  23. Jiang Y, Proteau P, Poulter D, Ferro-Novick S (1995) BTS1 encodes a geranylgeranyl diphosphate synthase in Saccharomyces cerevisiae. J Biol Chem 270(37):21793–21799PubMedCrossRefGoogle Scholar
  24. Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin Jrm, Rolland N (2009) Chloroplast proteomics and the compartmentation of plastidial isoprenoid biosynthetic pathways. Mol Plant 2(6):1154–1180PubMedCrossRefGoogle Scholar
  25. Kainou T, Kawamura K, Tanaka K, Matsuda H, Kawamukai M (1999) Identification of the GGPS1 genes encoding geranylgeranyl diphosphate synthases from mouse and human. Biochim Biophys Acta Mol Cell Biol Lipids 1437(3):333–340CrossRefGoogle Scholar
  26. Karimi M, De DeMeyer B, Hilson P (2005) Modular cloning in plant cells. Trends Plant Sci 10(3):103–105PubMedCrossRefGoogle Scholar
  27. Karlen Y, McNair A, Perseguers S, Mazza C, Mermod N (2007) Statistical significance of quantitative PCR. BMC Bioinformatics 8(1):131PubMedCrossRefGoogle Scholar
  28. Kellogg BA, Poulter CD (1997) Chain elongation in the isoprenoid biosynthetic pathway. Curr Opin Chem Biol 1(4):570–578PubMedCrossRefGoogle Scholar
  29. Koncz C, Shell C (1986) The promoter of T1-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by novel type of Agrobacterium binary vector. Mol Gen Genet 204:383–396CrossRefGoogle Scholar
  30. Kozak M (1997) Recognition of AUG and alternative initiator codons is augmented by G in position +4 but is not generally affected by the nucleotides in positions +5 and +6. EMBO J 16(9):2482–2492PubMedCrossRefGoogle Scholar
  31. Kuepfer L, Sauer U, Blank LM (2005) Metabolic functions of duplicate genes in Saccharomyces cerevisiae. Genome Res 15(10):1421–1430PubMedCrossRefGoogle Scholar
  32. Lange BM, Ghassemian M (2003) Genome organization in Arabidopsis thaliana: a survey for genes involved in isoprenoid and chlorophyll metabolism. Plant Mol Biol 51(6):925–948PubMedCrossRefGoogle Scholar
  33. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948PubMedCrossRefGoogle Scholar
  34. Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S, Drews GN, Fischer RL, Okamuro JK, Harada JJ, Goldberg RB (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci USA 107(18):8063–8070PubMedCrossRefGoogle Scholar
  35. Lefebvre V, North H, Frey A, Sotta B, Seo M, Okamoto M, Nambara E, Marion-Poll A (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J 45(3):309–319PubMedCrossRefGoogle Scholar
  36. Massonnet C, Vile D, Fabre J, Hannah MA, Caldana C, Lisec J, Beemster GT, Meyer RC, Messerli G, Gronlund JT, Perkovic J, Wigmore E, May S, Bevan MW, Meyer C, Rubio-Diaz S, Weigel D, Micol JL, Buchanan-Wollaston V, Fiorani F, Walsh S, Rinn B, Gruissem W, Hilson P, Hennig L, Willmitzer L, Granier C (2010) Probing the reproducibility of leaf growth and molecular phenotypes: a comparison of three Arabidopsis accessions cultivated in ten laboratories. Plant Physiol 152(4):2142–2157PubMedCrossRefGoogle Scholar
  37. Misawa N, Nakagawa M, Kobayashi K, Yamano S, Izawa Y, Nakamura K, Harashima K (1990) Elucidation of the Erwinia uredovora carotenoid biosynthetic pathway by functional analysis of gene products expressed in Escherichia coli. J Bacteriol 172(12):6704–6712PubMedGoogle Scholar
  38. Mitchum MG, Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, Kato T, Tabata S, Kamiya Y, Sun T-p (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J 45(5):804–818PubMedCrossRefGoogle Scholar
  39. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56(1):165–185PubMedCrossRefGoogle Scholar
  40. Nelson BK, Cai X, Nebenfuhr A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51(6):1126–1136PubMedCrossRefGoogle Scholar
  41. Nishino T, Rudney H (1977) Effects of detergents on the properties of 4-hydroxybenzoate. Polyprenyl transferase and the specificity of the polyprenyl pyrophosphate synthetic system in mitochondria. Biochemistry 16(4):605–609PubMedCrossRefGoogle Scholar
  42. Ohnuma S, Koyama T, Ogura K (1993) Alteration of the product specificities of prenyltransferases by metal ions. Biochem Bioph Res Co 192(2):407–412CrossRefGoogle Scholar
  43. Ohnuma S, Suzuki M, Nishino T (1994) Archaebacterial ether-linked lipid biosynthetic gene. Expression cloning, sequencing, and characterization of geranylgeranyl-diphosphate synthase. J Biol Chem 269(20):14792–14797PubMedGoogle Scholar
  44. Okada K, Saito T, Nakagawa T, Kawamukai M, Kamiya Y (2000) Five geranylgeranyl diphosphate synthases expressed in different organs are localized into three subcellular compartments in Arabidopsis. Plant Physiol 122(4):1045–1056PubMedCrossRefGoogle Scholar
  45. Pan J–J, Kuo T-H, Chen Y-K, Yang L-W, Po-Huang L (2002) Insight into the activation mechanism of Escherichia coli octaprenyl pyrophosphate synthase derived from pre-steady-state kinetic analysis. Biochim Biophys Acta Protein Struct Mol Enzymol 1594(1):64–73CrossRefGoogle Scholar
  46. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45Google Scholar
  47. Proost S, Van Bel M, Sterck L, Billiau K, Van Parys T, Van de Peer Y, Vandepoele K (2009) PLAZA: a comparative genomics resource to study gene and genome evolution in plants. Plant Cell 21(12):3718–3731PubMedCrossRefGoogle Scholar
  48. Rangan L, Vogel C, Srivastava A (2008) Analysis of context sequence surrounding translation initiation site from complete genome of model plants. Mol Biotechnol 39(3):207–213PubMedCrossRefGoogle Scholar
  49. Rieu I, Powers SJ (2009) Real-time quantitative RT-PCR: design, calculations, and statistics. Plant Cell 21(4):1031–1033PubMedCrossRefGoogle Scholar
  50. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37(6):e45PubMedCrossRefGoogle Scholar
  51. Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, Cardoso C, Lopez-Raez JA, Matusova R, Bours R, Verstappen F, Bouwmeester H (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155(2):721–734PubMedCrossRefGoogle Scholar
  52. Sandmann G, Misawa N, Wiedemann M, Vittorioso P, Carattoli A, Morelli G, Macino G (1993) Functional identification of al-3 from Neurospora crassa as the gene for geranylgeranyl pyrophosphate synthase by complementation with crt genes, in vitro characterization of the gene product and mutant analysis. J Photoch Photobio B 18(2–3):245–251CrossRefGoogle Scholar
  53. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37(5):501–506PubMedCrossRefGoogle Scholar
  54. Smyth D, Bowman J, Meyerowitz E (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767PubMedGoogle Scholar
  55. Tan B-C, Joseph LM, Deng W-T, Liu L, Li Q-B, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35(1):44–56PubMedCrossRefGoogle Scholar
  56. Tholl D, Lee S (2011) Terpene Specialized Metabolism in Arabidopsis thaliana. The Arabidopsis Book:e0143Google Scholar
  57. Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The botany array resource: e-Northerns, expression angling, and promoter analyses. Plant J 43(1):153–163PubMedCrossRefGoogle Scholar
  58. Ubeda-Tomas S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GTS, Hedden P, Bhalerao R, Bennett MJ (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 10(5):625–628PubMedCrossRefGoogle Scholar
  59. Ubeda-Tomás S, Federici F, Casimiro I, Beemster GTS, Bhalerao R, Swarup R, Doerner P, Haseloff J, Bennett MJ (2009) Gibberellin signaling in the endodermis controls arabidopsis root meristem size. Curr Biol 19(14):1194–1199PubMedCrossRefGoogle Scholar
  60. Vallon T, Ghanegaonkar S, Vielhauer O, Muller A, Albermann C, Sprenger G, Reuss M, Lemuth K (2008) Quantitative analysis of isoprenoid diphosphate intermediates in recombinant and wild-type Escherichia coli strains. Appl Microbiol Biotechnol 81(1):175–182PubMedCrossRefGoogle Scholar
  61. van Schie CC, Ament K, Schmidt A, Lange T, Haring MA, Schuurink RC (2007) Geranyl diphosphate synthase is required for biosynthesis of gibberellins. Plant J 52(4):752–762PubMedCrossRefGoogle Scholar
  62. Vandermoten S, Haubruge E, Cusson M (2009) New insights into short-chain prenyltransferases: structural features, evolutionary history and potential for selective inhibition. Cell Mol Life Sci 66(23):3685–3695Google Scholar
  63. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7):research0034.0031–research0034.0011Google Scholar
  64. Vranová E, Hirsch-Hoffmann M, Gruissem W (2011) AtIPD: a curated database of arabidopsis isoprenoid pathway models and genes for isoprenoid network analysis. Plant Physiol 156(4):1655–1660PubMedCrossRefGoogle Scholar
  65. Wang G, Dixon RA (2009) Heterodimeric geranyl(geranyl)diphosphate synthase from hop (Humulus lupulus) and the evolution of monoterpene biosynthesis. Proc Natl Acad Sci USA 106(24):9914–9919PubMedCrossRefGoogle Scholar
  66. Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59(1):225–251PubMedCrossRefGoogle Scholar
  67. Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18(6):292–298CrossRefGoogle Scholar
  68. Zhu X, Suzuki K, Okada K, Tanaka K, Nakagawa T, Kawamukai M, Matsuda K (1997a) Cloning and functional expression of a novel geranylgeranyl pyrophosphate synthase gene from Arabidopsis thaliana in Escherichia coli. Plant Cell Physiol 38(3):357–361PubMedCrossRefGoogle Scholar
  69. Zhu X, Suzuki K, Saito T, Okada K, Tanaka K, Nakagawa T, Matsuda H, Kawamukai M (1997b) Geranylgeranyl pyrophosphate synthase encoded by the newly isolated gene GGPS6 from Arabidopsis thaliana is localized in mitochondria. Plant Mol Biol 35(3):331–341PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Gilles Beck
    • 1
  • Diana Coman
    • 1
  • Edgar Herren
    • 1
  • M. Águila Ruiz-Sola
    • 2
  • Manuel Rodríguez-Concepción
    • 2
  • Wilhelm Gruissem
    • 1
  • Eva Vranová
    • 1
    • 3
  1. 1.Department of Biology, Plant BiotechnologyETH ZurichZurichSwitzerland
  2. 2.Department of Molecular GeneticsCentre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UBBarcelonaSpain
  3. 3.Faculty of Science, Institute of Biology and EcologyP. J. Šafárik University KošiceKošiceSlovakia

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