Plant Cell Reports

, Volume 37, Issue 8, pp 1113–1125 | Cite as

Isolation, characterization, and evaluation of three Citrus sinensis-derived constitutive gene promoters

  • L. Erpen
  • E. C. R. Tavano
  • R. Harakava
  • M. Dutt
  • J. W. Grosser
  • S. M. S. Piedade
  • B. M. J. Mendes
  • F. A. A. Mourão FilhoEmail author
Original Article


Key message

Regulatory sequences from the citrus constitutive genes cyclophilin (CsCYP), glyceraldehyde-3-phosphate dehydrogenase C2 (CsGAPC2), and elongation factor 1-alpha (CsEF1) were isolated, fused to the uidA gene, and qualitatively and quantitatively evaluated in transgenic sweet orange plants.


The 5′ upstream region of a gene (the promoter) is the most important component for the initiation and regulation of gene transcription of both native genes and transgenes in plants. The isolation and characterization of gene regulatory sequences are essential to the development of intragenic or cisgenic genetic manipulation strategies, which imply the use of genetic material from the same species or from closely related species. We describe herein the isolation and evaluation of the promoter sequence from three constitutively expressed citrus genes: cyclophilin (CsCYP), glyceraldehyde-3-phosphate dehydrogenase C2 (CsGAPC2), and elongation factor 1-alpha (CsEF1). The functionality of the promoters was confirmed by a histochemical GUS assay in leaves, stems, and roots of stably transformed citrus plants expressing the promoter-uidA construct. Lower uidA mRNA levels were detected when the transgene was under the control of citrus promoters as compared to the expression under the control of the CaMV35S promoter. The association of the uidA gene with the citrus-derived promoters resulted in mRNA levels of up to 60–41.8% of the value obtained with the construct containing CaMV35S driving the uidA gene. Moreover, a lower inter-individual variability in transgene expression was observed amongst the different transgenic lines, where gene constructs containing citrus-derived promoters were used. In silico analysis of the citrus-derived promoter sequences revealed that their activity may be controlled by several putative cis-regulatory elements. These citrus promoters will expand the availability of regulatory sequences for driving gene expression in citrus gene-modification programs.


Cis-regulatory elements Cultivar improvement Gene expression Sweet orange 



LE and ECRT acknowledge Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for research financial support and fellowships. BMJM, FAAMF, and LE acknowledge Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for research fellowships.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

299_2018_2298_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 23 KB)


  1. Anami S, Njuguna E, Coussens G, Aesaert S, Van Lijsebettens M (2013) Higher plant transformation: Principles and molecular tools. Int J Dev Biol 57:483–494CrossRefPubMedGoogle Scholar
  2. Andersen GR, Nissen P, Nyborg J (2003) Elongation factors in protein biosynthesis. Trends Biochem Sci 28:434–441CrossRefPubMedGoogle Scholar
  3. Azevedo FA, Mourão Filho FAA, Mendes BMJ, Almeida WAB, Schinor EH, Pio R, Barbosa JM, Guidetti-Gonzalez S, Carrer H, Lam E (2006a) Genetic transformation of Rangpur lime (Citrus limonia Osbeck) with the bO (bacterio-opsin) gene and its initial evaluation for Phytophthora nicotianae resistance. Plant Mol Biol Rep 24:185–196CrossRefGoogle Scholar
  4. Azevedo FA, Mourão Filho FAA, Schinor EH, Paoli LG, Mendes BMJ, Harakava R, Gabriel DW, Lee RF (2006b) GUS gene expression driven by a citrus promoter in transgenic tobacco and ‘Valencia’ sweet orange. Pesqui Agropecu Bras 41:1623–1628CrossRefGoogle Scholar
  5. Banerjee J, Sahoo DK, Raha S, Sarkar S, Dey N, Maiti IB (2015) A region containing an as-1 element of Dahlia mosaic virus (DaMV) subgenomic transcript promoter plays a key role in green tissue and root-specific expression in plants. Plant Mol Biol Rep 33:532–556CrossRefGoogle Scholar
  6. Bang SW, Park SH, Kim YS, Choi YD, Kim JK (2015) The activities of four constitutively expressed promoters in single-copy transgenic rice plants for two homozygous generations. Planta 241:1529–1541CrossRefPubMedGoogle Scholar
  7. Barbosa-Mendes JM, Mourão Filho FAA, Bergamin Filho A, Harakava R, Beer SV, Mendes BMJ (2009) Genetic transformation of Citrus sinensis cv. Hamlin with hrpN gene from Erwinia amylovora and evaluation of the transgenic lines for resistance to citrus canker. Sci Hortic 122:109–115CrossRefGoogle Scholar
  8. Benfey PN, Chua NH (1990) The cauliflower mosaic virus 35S promoter: combinatorial regulation of transcription in plants. Science 250:959–966CrossRefPubMedGoogle Scholar
  9. Benyon LS, Stover E, Bowman KD, Niedz R, Shatters RG Jr, Zale J, Belknap W (2013) GUS expression driven by constitutive and phloem-specific promoters in citrus hybrid US-802. Vitr Cell Dev Biol Plant 49:255–265CrossRefGoogle Scholar
  10. Beringer J, Chen W, Garton R, Sardesai N, Wang PH, Zhou N, Gupta M, Wu H (2017) Comparison of the impact of viral and plant-derived promoters regulating selectable marker gene on maize transformation and transgene expression. Plant Cell Rep 36:519–528CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bilas R, Szafran K, Hnatuszko-konka K (2016) Cis-regulatory elements used to control gene expression in plants. Plant Cell Tiss Org Cult 127:269–287CrossRefGoogle Scholar
  12. Boscariol RL, Monteiro M, Takahashi EK, Chabregas SM, Vieira MLC, Vieira LGE, Pereira LFP, Mourão Filho FAA, Cardoso SC, Christiano RSC, Bergamin Filho A, Barbosa JM, Azevedo FA, Mendes BMJ (2006) Attacin A gene from Tricloplusia ni reduces susceptibility to Xanthomonas axonopodis pv. citri in transgenic Citrus sinensis ‘Hamlin’. J Am Soc Hortic Sci 131:530–536Google Scholar
  13. Brasileiro MCA, Carneiro CTV (1998) Manual de transformação genética de plantas. Embrapa, BrasíliaGoogle Scholar
  14. Butaye KMJ, Cammue BPA, Delauré SL, De Bolle MFC (2005) Approaches to minimize variation of transgene expression in plants. Mol Breed 16:79–91CrossRefGoogle Scholar
  15. Butler JEF, Kadonaga JT (2002) The RNA polymerase II core promoter: a key component in the regulation of gene expression. Genes Dev 16:2583–2592CrossRefPubMedGoogle Scholar
  16. Cardoso SC, Barbosa-Mendes JM, Boscariol-Camargo RL, Christiano RSC, Bergamin Filho A, Vieira MLC, Mendes BMJ, Mourão Filho FAA (2010) Transgenic sweet orange (Citrus sinensis L. Osbeck) expressing the attacin A gene for resistance to Xanthomonas citri subsp. citri. Plant Mol Biol Rep 28:185–192CrossRefGoogle Scholar
  17. Carvalho RF, Folta KM (2017) Assessment of promoters and a selectable marker for development of strawberry intragenic vectors. Plant Cell Tiss Org Cult 128:259–271CrossRefGoogle Scholar
  18. Cervera M, Ortega C, Navarro A, Navarro L, Peña L (2000) Generation of transgenic citrus plants with the tolerance-to-salinity gene HAL2 from yeast. J Hortic Sci Biotechnol 75:26–30CrossRefGoogle Scholar
  19. Chakravarthi M, Syamaladevi DP, Harunipriya P, Augustine SM, Subramonian N (2016) A novel PR10 promoter from Erianthus arundinaceus directs high constitutive transgene expression and is enhanced upon wounding in heterologous plant systems. Mol Biol Rep 43:17–30CrossRefPubMedGoogle Scholar
  20. Chen Z, Wang J, Ye MX, Li H, Ji LX, Li Y, Cui DQ, Liu JM, An XM (2013) A novel moderate constitutive promoter derived from poplar (Populus tomentosa Carrière). Int J Mol Sci 14:6187–6204CrossRefPubMedPubMedCentralGoogle Scholar
  21. Correa MF, Pinto APC, Rezende JAM, Harakava R, Mendes BMJ (2015) Genetic transformation of sweet passion fruit (Passiflora alata) and reactions of the transgenic plants to Cowpea aphid borne mosaic virus. Eur J Plant Pathol 143:813–821CrossRefGoogle Scholar
  22. De Bolle MFC, Butaye KMJ, Coucke WJW, Goderis IJWM., Wouters PFJ, van Boxel N, Broekaert WF, Cammue BPA (2003) Analysis of the influence of promoter elements and a matrix attachment region on the inter-individual variation of transgene expression in populations of Arabidopsis thaliana. Plant Sci 165:169–179CrossRefGoogle Scholar
  23. Domínguez A, Guerri J, Cambra M, Navarro L, Moreno P, Peña L (2000) Efficient production of transgenic citrus plants expressing the coat protein gene of citrus tristeza virus. Plant Cell Rep 19:427–433CrossRefGoogle Scholar
  24. Domínguez A, Cervera M, Pérez RM, Romero J, Fagoaga C, Cubero J, López MM, Juárez J, Navarro L, Peña L (2004) Characterisation of regenerants obtained under selective conditions after Agrobacterium-mediated transformation of citrus explants reveals production of silenced and chimeric plants at unexpected high frequencies. Mol Breeding 14:171–183CrossRefGoogle Scholar
  25. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  26. Dutt M, Ananthakrishnan G, Jaromin MK, Brlansky RH, Grosser JW (2012) Evaluation of four phloem-specific promoters in vegetative tissues of transgenic citrus plants. Tree Physiol 32:83–93CrossRefPubMedGoogle Scholar
  27. Dutt M, Barthe G, Irey M, Grosser J (2015) Transgenic citrus expressing an Arabidopsis NPR1 gene exhibit enhanced resistance against Huanglongbing (HLB; Citrus greening). PLoS One 10:e0137134CrossRefPubMedPubMedCentralGoogle Scholar
  28. Espinoza C, Schlechter R, Herrera D, Torres E, Serrano A, Medina C, Arce-Johnson P (2013) Cisgenesis and intragenesis: new tools for improving crops. Biol Res 46:323–331CrossRefPubMedGoogle Scholar
  29. Galat A (1999) Variations of sequences and amino acid compositions of proteins that sustain their biological functions: An analysis of the cyclophilin family of proteins. Arch Biochem Biophys 371:149–162CrossRefPubMedGoogle Scholar
  30. Gambino G, Gribaudo I (2012) Genetic transformation of fruit trees: current status and remaining challenges. Transgenic Res 21:1163–1181CrossRefPubMedGoogle Scholar
  31. Gittins JR, Pellny TK, Hiles ER, Rosa C, Biricolti S, James DJ (2000) Transgene expression driven by heterologous ribulose-1,5-bisphosphate carboxylase/oxygenase small-subunit gene promoters in the vegetative tissues of apple (Malus pumila Mill.). Planta 210:232–240CrossRefPubMedGoogle Scholar
  32. Han YJ, Kim YM, Hwang OJ, Kim J-II (2015) Characterization of a small constitutive promoter from Arabidopsis translationally controlled tumor protein (AtTCTP) gene for plant transformation. Plant Cell Rep 34:265–275CrossRefPubMedGoogle Scholar
  33. He C, Lin Z, McElroy D, Wu R (2009) Identification of a rice Actin2 gene regulatory region for high-level expression of transgenes in monocots. Plant Biotechnol J 7:227–239CrossRefPubMedGoogle Scholar
  34. Hernandez-Garcia CM, Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Sci 217–218:109–119CrossRefPubMedGoogle Scholar
  35. Hernandez-Garcia CM, Martinelli AP, Bouchard RA, Finer JJ (2009) A soybean (Glycine max) polyubiquitin promoter gives strong constitutive expression in transgenic soybean. Plant Cell Rep 28:837–849CrossRefPubMedGoogle Scholar
  36. Hernandez-Garcia CM, Bouchard RA, Rushton PJ, Jones ML, Chen X, Timko MP, Finer JJ (2010) High level transgenic expression of soybean (Glycine max) GmERF and Gmubi gene promoters isolated by a novel promoter analysis pipeline. BMC Plant Biol 10:237CrossRefPubMedPubMedCentralGoogle Scholar
  37. Higo K, Ugawa Y, Iwamoto M, Korenaga (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300CrossRefPubMedPubMedCentralGoogle Scholar
  38. Holme IB, Wendt T, Holm PB (2013) Intragenesis and cisgenesis as alternatives to transgenic crop development. Plant Biotechnol J 11:395–407CrossRefPubMedGoogle Scholar
  39. Ishizaki K, Nonomura M, Kato H, Yamato KT, Kohchi T (2012) Visualization of auxin-mediated transcriptional activation using a common auxin-responsive reporter system in the liverwort Marchantia polymorpha. J Plant Res 125:643–651CrossRefPubMedGoogle Scholar
  40. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291CrossRefPubMedGoogle Scholar
  41. Kobayashi S, Uchimiya H (1989) Expression and integration of a foreign gene in orange (Citrus sinensis L. Osbeck.) protoplasts by direct DNA transfer. Jpn J Genet 64:91–97CrossRefGoogle Scholar
  42. Lam E, Benfey PN, Chua NH (1990) Characterization of as-1: a factor binding site on the 35S promoter of Cauliflower Mosaic Virus. In Lamb C, Beachy R (eds) Plant gene transfer. UCLA Symposium on Molecular Cell Biology, New Series. Wiley-Liss, Inc., New York, pp 71–79Google Scholar
  43. Lassen J, Madsen KH, Sandøe P (2002) Ethics and genetic engineering—lessons to be learned from GM foods. Bioproc Biosyst Eng 24:263–271CrossRefGoogle Scholar
  44. Li ZT, Kim KH, Jasinski JR, Creech MR, Gray DJ (2012) Large-scale characterization of promoters from grapevine (Vitis spp.) using quantitative anthocyanin and GUS assay systems. Plant Sci 196:132–142CrossRefPubMedGoogle Scholar
  45. Li Y, Liu X, Li J, Li S, Chen G, Zhou X, Yang W, Chen R (2015) Isolation of a maize ZmCI-1B promoter and characterization of its activity in transgenic maize and tobacco. Plant Cell Rep 34:1443–1457CrossRefPubMedGoogle Scholar
  46. Lu S, Zhang Y, Zheng X, Zhu K, Xu Q, Deng X (2016) Isolation and functional characterization of a lycopene-cyclase gene promoter from citrus. Front Plant Sci 7:1367PubMedPubMedCentralGoogle Scholar
  47. Mafra V, Kubo KS, Alves-Ferreira M, Ribeiro-Alves M, Stuart RM, Boava LP, Rodrigues CM, Machado MA (2012) Reference genes for accurate transcript normalization in citrus genotypes under different experimental conditions. PLoS One 7:e31263CrossRefPubMedPubMedCentralGoogle Scholar
  48. Malnoy M, Venisse J, Reynoird J, Chevreau E (2003) Activation of three pathogen-inducible promoters of tobacco in transgenic pear (Pyrus communis L.) after abiotic and biotic elicitation. Planta 216:802–814PubMedGoogle Scholar
  49. Malnoy M, Reynoird J, Borejsza-Wysocka EE, Aldwinckle HS (2006) Activation of the pathogen-inducible Gst1 promoter of potato after elicitation by Venturia inaequalis and Erwinia amylovora in transgenic apple (Malus x domestica). Transgenic Res 15:83–93CrossRefPubMedGoogle Scholar
  50. Mendes BMJ, Cardoso SC, Boscariol-Camargo RL, Cruz RB, Mourão Filho FAA, Bergamin Filho A (2010) Reduction in susceptibility to Xanthomonas axonopodis pv. citri in transgenic Citrus sinensis expressing the rice Xa21 gene. Plant Pathol 59:68–75CrossRefGoogle Scholar
  51. Merrick WC (1992) Mechanism and regulation of eukaryotic protein synthesis. Microbiol Rev 56:291–315PubMedPubMedCentralGoogle Scholar
  52. Meyer P, Saedler H (1996) Homology-dependent gene silencing in plants. Annu Rev Plant Phys 47:23–48CrossRefGoogle Scholar
  53. Miyata LY, Harakava R, Stipp LCL, Mendes BM, Appezzato-da-Glória B, Mourão Filho FAA (2012) GUS expression in sweet oranges (Citrus sinensis L. Osbeck) driven by three different phloem-specific promoters. Plant Cell Rep 31:2005–2013CrossRefPubMedGoogle Scholar
  54. Molinari HBC, Marur CJ, Filho JCB, Kobayashi AK, Pileggi M, Leite Júnior RP, Pereira LFP, Vieira LGE (2004) Osmotic adjustment in transgenic citrus rootstock Carrizo citrange (Citrus sinensis Osb. x Poncirus trifoliata L. Raf.) overproducing proline. Plant Sci 167:1375–1381CrossRefGoogle Scholar
  55. Muniz FR, De Souza AJ, Stipp LCL, Schinor E, Freitas W Jr, Harakava R, Stach-Machado DR, Rezende JAM, Mourão Filho FAA, Mendes BMJ (2012) Genetic transformation of Citrus sinensis with Citrus tristeza virus (CTV) derived sequences and reaction of transgenic lines to CTV infection. Biol Plant 56:162–166CrossRefGoogle Scholar
  56. Muñoz-Bertomeu J, Cascales-Miñana B, Mulet JM, Baroja-Fernández E, Pozueta-Romero J, Kuhn JM, Segura J, Ros R (2009) Plastidial glyceraldehyde-3-phosphate dehydrogenase deficiency leads to altered root development and affects the sugar and amino acid balance in Arabidopsis. Plant Physiol 151:541–558CrossRefPubMedPubMedCentralGoogle Scholar
  57. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  58. Murashige T, Tucker DPH (1969) Growth factor requirement of citrus tissue culture. In: International Citrus Symposium. University of California, Riverside, pp 1155–1169Google Scholar
  59. Odell JT, Nagy F, Chua NH (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313:47–48CrossRefGoogle Scholar
  60. Paoli LG, Boscariol-Camargo RL, Harakava R, Mendes BMJ, Mourão Filho FAA (2007) Transformação genética de laranja ‘Valencia’ com o gene cecropin MB39. Pesqui Agropecu Bras 42:1663–1666CrossRefGoogle Scholar
  61. Park SH, Yi N, Kim YS, Jeong MH, Bang SW, Choi YD, Kim JK (2010) Analysis of five novel putative constitutive gene promoters in transgenic rice plants. J Exp Bot 61:2459–2467CrossRefPubMedPubMedCentralGoogle Scholar
  62. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45CrossRefPubMedPubMedCentralGoogle Scholar
  63. Philip A, Syamaladevi DP, Chakravarthi M, Gopinath K, Subramonian N (2013) 5′ Regulatory region of ubiquitin 2 gene from Porteresia coarctata makes efficient promoters for transgene expression in monocots and dicots. Plant Cell Rep 32:1199–1210CrossRefPubMedGoogle Scholar
  64. Porto MS, Pinheiro MPN, Batista VGL, dos Santos RC, Filho Pde A, de Lima LM (2014) Plant promoters: An approach of structure and function. Mol Biotechnol 56:38–49CrossRefPubMedGoogle Scholar
  65. Potenza C, Aleman L, Sengupta-Gopalan C (2004) Targeting transgene expression in research, agricultural, and environmental applications: promoters used in plant transformation. In Vitro Cell Dev-Pl 40:1–22CrossRefGoogle Scholar
  66. Ramakers C, Ruijter JM, Lekanne Deprez RH, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66CrossRefPubMedGoogle Scholar
  67. Reyes JC, Muro-Pastor MI, Florencio FJ (2004) The GATA family of transcription factors in Arabidopsis and rice. Plant Physiol 134:1718–1732CrossRefPubMedPubMedCentralGoogle Scholar
  68. Rius SP, Casati P, Iglesias AA, Gomez-Casati DF (2008) Characterization of Arabidopsis lines deficient in GAPC-1, a cytosolic NAD-dependent glyceraldehyde-3-phosphate dehydrogenase. Plant Physiol 148:1655–1667CrossRefPubMedPubMedCentralGoogle Scholar
  69. Romano PGN, Horton P, Gray JE (2004) The Arabidopsis cyclophilin gene family. Plant Physiol 134:1268–1282CrossRefPubMedPubMedCentralGoogle Scholar
  70. Schaart JG, Van de Wiel CCM, Lotz LAP, Smulders MJM (2016) Opportunities for products of new plant breeding techniques. Trends Plant Sci 21:438–449CrossRefPubMedGoogle Scholar
  71. Singh S, Rajam MV (2009) Citrus biotechnology: achievements, limitations and future directions. Physiol Mol Biol Plants 15:3–22CrossRefPubMedPubMedCentralGoogle Scholar
  72. Sorkina A, Bardosh G, Liu YZ, Fridman I, Schlizerman L, Zur N, Or E, Goldschmidt EE, Blumwald E, Sadka A (2011) Isolation of a citrus promoter specific for reproductive organs and its functional analysis in isolated juice sacs and tomato. Plant Cell Rep 30:1627–1640CrossRefPubMedGoogle Scholar
  73. Suhandono S, Apriyanto A, Ihsani N (2014) Isolation and characterization of three cassava elongation factor 1 alpha (MeEF1A) promoters. PLoS One 9:32–34CrossRefGoogle Scholar
  74. Tavano ECR, Vieira MLC, Mourão Filho FAA, Harakava R, Mendes BMJ (2015) Genetic transformation of Citrus Sinensis “Hamlin” with Attacin a driven by a phloem tissue-specific promoter for resistance to Candidatus Liberibacter spp. Acta Hortic 1065:695–702CrossRefGoogle Scholar
  75. Teakle GR, Manfield IW, Graham JF, Gilmartin PM (2002) Arabidopsis thaliana GATA factors: organization, expression and DNA-binding characteristics. Plant Mol Biol 50:43–57CrossRefPubMedGoogle Scholar
  76. Verdaguer B, De Kochko A, Fux CI, Beachy RN, Fauquet C (1998) Functional organization of the cassava vein mosaic virus (CsVMV) promoter. Plant Mol Biol 37:1055–1067CrossRefPubMedGoogle Scholar
  77. Xiao K, Zhang C, Harrison M, Wang ZY (2005) Isolation and characterization of a novel plant promoter that directs strong constitutive expression of transgenes in plants. Mol Breed 15:221–231CrossRefGoogle Scholar
  78. Yang L, Hu C, Li N, Zhang J, Yan J, Deng Z (2011) Transformation of sweet orange [Citrus sinensis (L.) Osbeck] with pthA-nls for acquiring resistance to citrus canker disease. Plant Mol Biol 75:11–23CrossRefPubMedGoogle Scholar
  79. Zhang N, McHale LK, Finer JJ (2015) Isolation and characterization of “GmScream” promoters that regulate highly expressing soybean (Glycine max Merr.) genes. Plant Sci 241:189–198CrossRefPubMedGoogle Scholar
  80. Zhou J, Yang Y, Wang X, Yu F, Yu C, Chen J, Cheng Y, Yan C (2013) Enhanced transgene expression in rice following selection controlled by weak promoters. BMC Biotechnol 13:29CrossRefPubMedPubMedCentralGoogle Scholar
  81. Zou X, Song E, Peng A, He Y, Xu L, Lei T, Yao L, Chen S (2014) Activation of three pathogen inducible promoters in transgenic citrus (Citrus sinensis Osbeck) after Xanthomonas axonopodis pv. citri infection and wounding. Plant Cell Tiss Org Cult 117:85–98CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • L. Erpen
    • 1
  • E. C. R. Tavano
    • 2
  • R. Harakava
    • 3
  • M. Dutt
    • 4
  • J. W. Grosser
    • 4
  • S. M. S. Piedade
    • 1
  • B. M. J. Mendes
    • 2
  • F. A. A. Mourão Filho
    • 1
    Email author
  1. 1.Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São PauloPiracicabaBrazil
  2. 2.Centro de Energia Nuclear na Agricultura, Universidade de São PauloPiracicabaBrazil
  3. 3.Instituto BiológicoSão PauloBrazil
  4. 4.Citrus Research and Education CenterUniversity of FloridaLake AlfredUSA

Personalised recommendations