Advertisement

Promoter Analysis in Banana

  • Efrén SantosEmail author
  • Ricardo Pacheco
  • Liliana Villao
  • Luis Galarza
  • Daniel Ochoa
  • Carlos Jordán
  • José Flores
Chapter

Abstract

Currently, several research laboratories are developing genetically modified bananas and plantains for different purposes, while new transgenic crops are being developed and released in several countries. Therefore, a more regulated transgene expression is needed. Furthermore, native banana promoters should imply a more public acceptance than heterologous sequences. Promoter isolation could be performed by an insertional mutagenesis approach or indirectly by analyzing expression patterns of related genes. Advances in genomics led to the genome sequencing and gene annotation of banana, as a source to identify candidate promoters for specific expression patterns. The challenge in computational approaches for promoter characterization is to precisely identify pattern of expression. Actually, promoter analysis for activity characterization has been confirmed through experimentation with different techniques, including reporter genes, bioinformatics analysis for candidate cis-acting element and promoter prediction, and expression analysis of related genes. A review of characterization of different banana promoters is summarized, and the analysis of available banana promoter sequences in the GenBank was performed with available bioinformatics tools and a novel method to identify motif sequences. Furthermore, a list of promoters used in the development of genetically modified banana is presented, indicating an increase of plant and native banana promoters used to drive expression of related gene in a specific pattern.

Keywords

Regulatory sequence Reporter genes In silico Bioinformatics Musa Gene expression Promoter tagging 

Notes

Acknowledgments

Promoter activity in banana transgenic lines was performed in the framework of the SENESCYT project: PIC-08-0000300.

References

  1. André D, Colau D, Schell J, Montagu M, Hernalsteens JP (1986) Gene tagging in plants by a T-DNA insertion mutagen that generates APH(3′)II-plant gene fusions. Mol Gen Genet 204:512–518CrossRefGoogle Scholar
  2. Asif M, Lakhwani D, Pathak S et al (2014) Genome-wide identification and expression analysis of the mitogen-activated protein kinase gene family from banana suggest involvement of specific members in different stages of fruit ripening. Funct Integr Genomics 14(1):161–175. doi: 10.1007/s10142-013-0349-9 PubMedCrossRefGoogle Scholar
  3. Atkinson HJ, Grimwood S, Johnston K, Green J (2004) Prototype demonstration of transgenic resistance to the nematode Radopholus similis conferred on banana by a cystatin. Transgenic Res 13:135–142PubMedCrossRefGoogle Scholar
  4. Ba L, Shan W, Kuang J et al (2014a) The banana MaLBD (lateral organ boundaries domain) transcription factors regulate EXPANSIN expression and are involved in fruit ripening. Plant Mol Biol Report 32(6):1103–1113. doi: 10.1007/s11105-014-0720-6 CrossRefGoogle Scholar
  5. Ba L, Shan W, Xiao Y et al (2014b) A ripening-induced transcription factor MaBSD1 interacts with promoters of MaEXP1/2 from banana fruit. Plant Cell Rep 33(11):1913–1920. doi: 10.1007/s00299-014-1668-6 PubMedCrossRefGoogle Scholar
  6. Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373PubMedPubMedCentralCrossRefGoogle Scholar
  7. Berk AJ (1999) Activation of RNA polymerase II transcription. Curr Opin Cell Biol 11:330–335PubMedCrossRefGoogle Scholar
  8. Breathnach R, Chambon P (1981) Organization and expression of eukaryotic split genes-coding for proteins. Annu Rev Biochem 50:349–383PubMedCrossRefGoogle Scholar
  9. Calderon-Villalobos LIA, Kuhnle C, Li HB, Rosso M, Weisshaar B, Schwechheimer C (2006) LucTrap vectors are tools to generate luciferase fusions for the quantification of transcript and protein abundance in vivo. Plant Physiol 141:3–14PubMedPubMedCentralCrossRefGoogle Scholar
  10. Castle J, Szekeres M, Jenkins G, Bishop GJ (2005) Unique and overlapping expression patterns of Arabidopsis CYP85 genes involved in brassinosteroid C-6 oxidation. Plant Mol Biol 57:129–140PubMedCrossRefGoogle Scholar
  11. Chakrabarti A, Ganapathi TR, Mukherjee PK, Bapat VA (2003) MSI-99, a magainin analogue, imparts enhanced disease resistance in transgenic tobacco and banana. Planta 216:587–596PubMedGoogle Scholar
  12. Chiu WL, Niwa Y, Zeng W, Hirano T, Kobayashi H, Sheen J (1996) Engineered GFP as a vital reporter in plants. Curr Biol 6:325–330PubMedCrossRefGoogle Scholar
  13. Chong-Pérez B, Kosky RG, Reyes M et al (2012) Heat shock induced excision of selectable marker genes in transgenic banana by the Cre-lox site-specific recombination system. J Biotechnol 159(4):265–273. doi: 10.1016/j.jbiotec.2011.07.031 PubMedCrossRefGoogle Scholar
  14. Chong-Pérez B, Reyes M, Rojas L, Ocaña B et al (2013) Excision of a selectable marker gene in transgenic banana using a Cre/lox system controlled by an embryo specific promoter. Plant Mol Biol 83:143–152. doi: 10.1007/s11103-013-0058-8 PubMedCrossRefGoogle Scholar
  15. Christensen AH, Sharrock RA, Quail PH (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18:675–689PubMedCrossRefGoogle Scholar
  16. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190PubMedPubMedCentralCrossRefGoogle Scholar
  17. Droc G, Lariviere D, Guignon V et al (2013) The banana genome hub. Database 2013:bat035. doi: 10.1093/database/bat035
  18. Dugdale B, Beetham PR, Becker DK, Harding RM, Dale JL (1998) Promoter activity associated with the intergenic regions of banana bunchy top virus DNA-1 to-6 in transgenic tobacco and banana cells. J Gen Virol 79:2301–2311PubMedCrossRefGoogle Scholar
  19. Dugdale B, Becker DK, Harding RM, Dale JL (2001) Intron-mediated enhancement of the banana bunchy top virus DNA-6 promoter in banana (Musa spp.) embryogenic cells and plants. Plant Cell Rep 20:220–226CrossRefGoogle Scholar
  20. Dynan WS (1986) Promoters for housekeeping genes. Trends Genet 2:196–197CrossRefGoogle Scholar
  21. Elliott AR, Campbell JA, Dugdale B, Brettell RIS, Grof CPL (1999) Green fluorescent protein facilitates rapid in vivo detection of genetically transformed plant cells. Plant Cell Rep 18:707–714CrossRefGoogle Scholar
  22. Feldmann KA (1991) T-DNA insertion mutagenesis in Arabidopsis: mutational spectrum. Plant J 1:71–82CrossRefGoogle Scholar
  23. Fobert PR, Miki BL, Iyer VN (1991) Detection of gene regulatory signals in plants revealed by T-DNA-mediated fusions. Plant Mol Biol 17:837–851PubMedCrossRefGoogle Scholar
  24. Fobert PR, Labbe H, Cosmopoulos J et al (1994) T-DNA tagging of a seed coat-specific cryptic promoter in tobacco. Plant J 6:567–577PubMedCrossRefGoogle Scholar
  25. Ghosh A, Shekhawat U, Ganapathi T et al (2012) Analysis of banana fruit-specific promoters using transient expression in embryogenic cells of banana cultivar Robusta (AAA Group). J Plant Biochem Biotechnol 21(2):189–197. doi: 10.1007/s13562-011-0070-5 CrossRefGoogle Scholar
  26. Halfon MS (2006) (Re)modeling the transcriptional enhancer. Nat Genet 38:1102–1103PubMedCrossRefGoogle Scholar
  27. He S, Shan W, Kuang J et al (2013) Molecular characterization of a stress-response bZIP transcription factor in banana. Plant Cell Tiss Org Cult 113(2):173–187. doi: 10.1007/s11240-012-0258-y CrossRefGoogle Scholar
  28. Heim R, Cubitt AB, Tsien RY (1995) Improved green fluorescence. Nature 373:663–664PubMedCrossRefGoogle Scholar
  29. Hermann SR, Harding RM, Dale JL (2001) The banana actin 1 promoter drives near-constitutive transgene expression in vegetative tissues of banana (Musa spp.). Plant Cell Rep 20:525–530CrossRefGoogle Scholar
  30. Hernandez-Garcia CM, Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Sci 217–218:109–119PubMedCrossRefGoogle Scholar
  31. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300PubMedPubMedCentralCrossRefGoogle Scholar
  32. Hraska M, Rakousky S, Curn V (2006) Green fluorescent protein as a vital marker for non-destructive detection of transformation events in transgenic plants. Plant Cell Tiss Org Cult 86:303–318CrossRefGoogle Scholar
  33. Janssens H, Hou SL, Jaeger J et al (2006) Quantitative and predictive model of transcriptional control of the Drosophila melanogaster even skipped gene. Nat Genet 38:1159–1165PubMedCrossRefGoogle Scholar
  34. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907PubMedPubMedCentralGoogle Scholar
  35. Jordan CI, Jordan CJ (2015) MBMEDA: an application of estimation of distribution algorithms to the problem of finding biological motifs. Lecture notes in computer science. Artificial computation in biology and medicine, vol 9107. Springer International Publishing, Cham, pp 39–46Google Scholar
  36. Kankainen M, Holm L (2005) POCO: discovery of regulatory patterns from promoters of oppositely expressed gene sets. Nucleic Acids Res 33(Web Server issue):W427–W431Google Scholar
  37. Kertbundit S, De Greve H, Deboeck F, Van Montagu M, Hernalsteens JP (1991) In vivo random β-glucuronidase gene fusions in Arabidopsis thaliana. Proc Natl Acad Sci U S A 88:5212–5216PubMedPubMedCentralCrossRefGoogle Scholar
  38. Koncz C, Martini N, Mayerhofer R et al (1989) High-frequency T-DNA-mediated gene tagging in plants. Proc Natl Acad Sci U S A 86:8467–8471PubMedPubMedCentralCrossRefGoogle Scholar
  39. Kristiansson E, Thorsen M, Tamás MJ, Nerman O (2009) Evolutionary forces act on promoter length: identification of enriched Cis-regulatory elements. Mol Biol Evol 26(6):1299–1307. doi: 10.1093/molbev/msp040 PubMedCrossRefGoogle Scholar
  40. Krysan PJ, Young JC, Sussman MR (1999) T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11:2283–2290PubMedPubMedCentralCrossRefGoogle Scholar
  41. Kuang J, Chen L, Shan W et al (2013) Molecular characterization of two banana ethylene signaling component MaEBFs during fruit ripening. Postharvest Biol Technol 85:94–101. doi: 10.1016/j.postharvbio.2013.05.004 CrossRefGoogle Scholar
  42. Kumari S, Ware D (2013) Genome-wide computational prediction and analysis of core promoter elements across plant monocots and dicots. PLoS One 8(10):e79011PubMedPubMedCentralCrossRefGoogle Scholar
  43. Kutach AK, Kadonaga JT (2000) The downstream promoter element DPE appears to be as widely used as the TATA box in Drosophila core promoters. Mol Cell Biol 20:4754–4764PubMedPubMedCentralCrossRefGoogle Scholar
  44. Lee TI, Young RA (2000) Transcription of eukaryotic protein-coding genes. Annu Rev Genet 34:77–137PubMedCrossRefGoogle Scholar
  45. Lescot M, Dehais P, Thijs G 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 30:325–327PubMedPubMedCentralCrossRefGoogle Scholar
  46. Liu X, Brutlag DL, Liu JS (2001) Bioprospector: discovering conserved DNa motifs in upstream regulatory regions of co-expressed genes. Pac Symp Biocomput 6:127–138Google Scholar
  47. Liu J, Liu L, Li Y et al (2015) Role for the banana AGAMOUS-like gene MaMADS7 in regulation of fruit ripening and quality. Physiol Plant 155(3):217–231PubMedCrossRefGoogle Scholar
  48. Mandal A, Sandgren M, Holmstrom KO, Gallois P, Palva ET (1995) Identification of Arabidopsis thaliana sequences responsive to low temperature and abscisic acid by T-DNA tagging and in-vivo gene fusion. Plant Mol Biol Report 13:243–254CrossRefGoogle Scholar
  49. Marilley M, Pasero P (1996) Common DNA structural features exhibited by eukaryotic ribosomal gene promoters. Nucleic Acids Res 24:2204–2211PubMedPubMedCentralCrossRefGoogle Scholar
  50. Martienssen RA (1998) Functional genomics: probing plant gene function and expression with transposons. Proc Natl Acad Sci U S A 95:2021–2026PubMedPubMedCentralCrossRefGoogle Scholar
  51. Maruyama K, Todaka D, Mizoi J et al (2012) Identification of Cis-acting promoter elements in cold- and dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res 19(1):37–49. doi: 10.1093/dnares/dsr040 PubMedCrossRefGoogle Scholar
  52. Matsumoto K, Morais LS, Vianna GR, Aragão FJL, Rech EL (2002) Genetic transformation of banana embryogenic cells through particle bombardment using a herbicide resistance gene as selectable marker. Acta Horticult 575:61–67CrossRefGoogle Scholar
  53. Maximova SN, Dandekar AM, Guiltinan MJ (1998) Investigation of Agrobacterium-mediated transformation of apple using green fluorescent protein: high transient expression and low stable transformation suggest that factors other than T-DNA transfer are rate-limiting. Plant Mol Biol 37:549–559PubMedCrossRefGoogle Scholar
  54. May GD, Afza R, Mason HS et al (1995) Generation of transgenic banana (Musa acuminata) plants via Agrobacterium-mediated transformation. Biotechnology 13:486–492CrossRefGoogle Scholar
  55. Mellor J (2006) Dynamic nucleosomes and gene transcription. Trends Genet 22:320–329PubMedCrossRefGoogle Scholar
  56. Mollier P, Hoffmann B, Orsel M, Pelletier G (2000) Tagging of a cryptic promoter that confers root-specific gus expression in Arabidopsis thaliana. Plant Cell Rep 19:1076–1083CrossRefGoogle Scholar
  57. Mudge SR, Birch RG (1998) T-DNA tagging and characterisation of a novel meristem-specific promoter from tobacco. Aust J Plant Physiol 25:637–643CrossRefGoogle Scholar
  58. Nakamura M, Tsunoda T, Obokata J (2002) Photosynthesis nuclear genes generally lack TATA-boxes: a tobacco photosystem I gene responds to light through an initiator. Plant J 29:1–10PubMedCrossRefGoogle Scholar
  59. Ökrész L, Mathe C, Horvath E et al (1998) T-DNA trapping of a cryptic promoter identifies an ortholog of highly conserved SNZ growth arrest response genes in Arabidopsis. Plant Sci 138:217–228CrossRefGoogle Scholar
  60. Ow DW, Wood KW, DeLuca M et al (1986) Transient and stable expression of the firefly luciferase gene in plant cells and transgenic plants and transgenic plants. Science 234:856–859PubMedCrossRefGoogle Scholar
  61. Pandey SP, Krishnamachari A (2006) Computational analysis of plant RNA Pol-II promoters. Biosystems 83:38–50PubMedCrossRefGoogle Scholar
  62. Peng H, Shan W, Kuang J et al (2013) Molecular characterization of cold-responsive basic helix-loop-helix transcription factors MabHLHs that interact with MaICE1 in banana fruit. Planta 238(5):937–953. doi: 10.1007/s00425-013-1944-7 PubMedCrossRefGoogle Scholar
  63. Plesch G, Kamann E, Mueller-Roeber B (2000) Cloning of regulatory sequences mediating guard-cell-specific gene expression. Gene 249:83–89PubMedCrossRefGoogle Scholar
  64. Praz V, Perier R, Bonnard C, Bucher P (2002) The eukaryotic promoter database, EPD: new entry types and links to gene expression data. Nucleic Acids Res 30:322–324PubMedPubMedCentralCrossRefGoogle Scholar
  65. Radhamony RN, Prasad AM, Srinivasan R (2005) T-DNA insertional mutagenesis in Arabidopsis: a tool for functional genomics. Electron J Biotechnol 8:82–106Google Scholar
  66. Remy S (2000) Genetic transformation of banana (Musa spp.) for disease resistance by expression of antimicrobial proteins. Dissertationes de agricultura. Ph.D. thesis 420.KatholiekeUniversiteit Leuven, Belgium. Faculteit Bio-ingenieurswetenschappen. 341 pGoogle Scholar
  67. Remy S, Buyens A, Cammue BPA, Swennen R, Sági L (1998) Production of transgenic banana plants expressing antifungal proteins. Acta Horticult 490:433–436CrossRefGoogle Scholar
  68. Remy S, De Weerdt G, Deconinck I, Swennen R, Sági L (2004) An ultrasensitive luminescent detection system in banana biotechnology: from promoter tagging to southern hybridization. In: Mohan Jain S, Swennen R (eds) Banana improvement: cellular, molecular biology, and induced mutations. Science Publishers, Enfield, pp 307–319Google Scholar
  69. Remy S, Thiry E, Coemans B et al (2005) Improved T-DNA vector for tagging plant promoters via high-throughput luciferase screening. Biotechniques 38:763–770PubMedCrossRefGoogle Scholar
  70. Rombauts S, Florquin K, Lescot M et al (2003) Computational approaches to identify promoters and cis-regulatory elements in plant genomes. Plant Physiol 132:1162–1176PubMedPubMedCentralCrossRefGoogle Scholar
  71. Roy Choudhury S, Roy S, Das R, Sengupta DN (2008a) Differential transcriptional regulation of banana sucrose phosphate synthase gene in response to ethylene, auxin, wounding, low temperature and different photoperiods during fruit ripening and functional analysis of banana SPS gene promoter. Planta 229:207–223. doi: 10.1007/s00425-008-0821-2 PubMedCrossRefGoogle Scholar
  72. Roy Choudhury S, Roy S, ParamitaSaha P, Kumar Singh S, Sengupta DN (2008b) Characterization of differential ripening pattern in association with ethylene biosynthesis in the fruits of five naturally occurring banana cultivars and detection of a GCC-box-specific DNA-binding protein. Plant Cell Rep 27:1235–1249. doi: 10.1007/s00299-008-0547-4 CrossRefGoogle Scholar
  73. Roy Choudhury S, Roy S, Sengupta DN (2009) A comparative study of cultivar differences in sucrose phosphate synthase gene expression and sucrose formation during banana fruit ripening. Postharvest Biol Technol 54(1):15–24. doi: 10.1016/j.postharvbio.2009.05.003 CrossRefGoogle Scholar
  74. Roy Choudhury S, Roy S, Singh S, Sengupta D (2010) Understanding the molecular mechanism of transcriptional regulation of banana Sucrose phosphate synthase (SPS) gene during fruit ripening: an insight into the functions of various cis-acting regulatory elements. Plant Signal Behav 5(5):553–557. doi: 10.4161/psb.11092 CrossRefGoogle Scholar
  75. Roy Choudhury S, Roy S, Singh K, Sengupta DN (2011) Ma-ACS1: a key operator in ethylene biosynthesis in banana – its role and regulation during fruit ripening. Acta Horticult 897:187–194CrossRefGoogle Scholar
  76. Sági L, Remy S, Panis B, Volckaert G, Swennen R (1992) Transient gene expression in banana protoplasts. Banana Newslett 15:42Google Scholar
  77. Sági L, Panis B, Remy S et al (1995) Genetic transformation of banana and plantain (Musa spp.) via particle bombardment. Biotechnology 13:481–485PubMedCrossRefGoogle Scholar
  78. Santos Ordóñez EG (2008) Characterization and isolation of T-DNA tagged banana promoters active during in vitro regeneration and low temperature stress. Dissertationes de agricultura. Ph.D. thesis 787.KatholiekeUniversiteit Leuven, Belgium. Faculteit Bio-Ingenieurswetenschappen, 188 pGoogle Scholar
  79. Santos E, Remy R, Thiry E et al (2009) Characterization and isolation of a T-DNA tagged banana promoter active during in vitro culture and low temperature stress. BMC Plant Biol 9:77. doi: 10.1186/1471-2229-9-77 PubMedPubMedCentralCrossRefGoogle Scholar
  80. Schatz T, Langowski J (1997) Curvature and sequence analysis of eukaryotic promoters. J Biomol Struct Dyn 15:265–275PubMedCrossRefGoogle Scholar
  81. Schenk PM, Sági L, Remans T et al (1999) A promoter from sugarcane bacilliform badnavirus drives transgene expression in banana and other monocot and dicot plants. Plant Mol Biol 39:1221–1230PubMedCrossRefGoogle Scholar
  82. Schenk PM, Remans T, Sági L et al (2001) Promoters for pregenomic RNA of banana streak badnavirus are active for transgene expression in monocot and dicot plants. Plant Mol Biol 47:399–412PubMedCrossRefGoogle Scholar
  83. Schneider TD, Stephens RM (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18:6097–6100PubMedPubMedCentralCrossRefGoogle Scholar
  84. Seki M, Narusaka M, Kamiya A et al (2002) Functional annotation of a full-length Arabidopsis cDNA collection. Science 296:141–145PubMedCrossRefGoogle Scholar
  85. Shahmuradov IA, Gammerman AJ, Hancock JM, Bramley PM, Solovyev VV (2003) PlantProm: a database of plant promoter sequences. Nucleic Acids Res 31:114–117PubMedPubMedCentralCrossRefGoogle Scholar
  86. Shahmuradov IA, Solovyev VV, Gammerman AJ (2005) Plant promoter prediction with confidence estimation. Nucleic Acids Res 33:1069–1076PubMedPubMedCentralCrossRefGoogle Scholar
  87. Shan W, Kuang J, Chen L et al (2012) Molecular characterization of banana NAC transcription factors and their interactions with ethylene signalling component EIL during fruit ripening. J Exp Bot 63(14):5171–5187. doi: 10.1093/jxb/ers178 PubMedPubMedCentralCrossRefGoogle Scholar
  88. Shan W, Kuang J, Lu W et al (2014) Banana fruit NAC transcription factor MaNAC1 is a direct target of MaICE1 and involved in cold stress through interacting with MaCBF1. Plant Cell Environ 37(9):2116–2127. doi: 10.1111/pce.12303 PubMedCrossRefGoogle Scholar
  89. Shekhawat U, Srinivas L, Ganapathi T (2011) MusaDHN-1, a novel multiple stress-inducible SK3-type dehydrin gene, contributes affirmatively to drought- and salt-stress tolerance in banana. Planta 234(5):915–932. doi: 10.1007/s00425-011-1455-3 PubMedCrossRefGoogle Scholar
  90. Sivanandan C, Sujatha TP, Prasad AM et al (2005) T-DNA tagging and characterization of a cryptic root-specific promoter in Arabidopsis. Biochim Biophys Acta-Gene Struct Expr 1731:202–208CrossRefGoogle Scholar
  91. Smale ST (1994) Core promoter architecture for eucaryotic protein-coding genes. In: Conaway RC, Conaway JW (eds) Transcription: mechanisms and regulation. Raven Press, Ltd., New York, pp 63–81Google Scholar
  92. Smale ST (1997) Transcription initiation from TATA-less promoters within eukaryotic protein-coding genes. Biochim Biophys Acta-Gene Struct Expr 1351:73–88CrossRefGoogle Scholar
  93. Smale ST, Kadonaga JT (2003) The RNA polymerase II core promoter. Annu Rev Biochem 72:449–479PubMedCrossRefGoogle Scholar
  94. Springer PS (2000) Gene traps: tools for plant development and genomics. Plant Cell 12:1007–1020PubMedPubMedCentralCrossRefGoogle Scholar
  95. Sreedharan S, Singh Shekhawat UK, Ganapathi TR (2015) Constitutive and stress‑inducible overexpression of a native aquaporin gene (MusaPIP2;6) in transgenic banana plants signals its pivotal role in salt tolerance. Plant Mol Biol 88:41–52. doi: 10.1007/s11103-015-0305-2 PubMedCrossRefGoogle Scholar
  96. Struhl K (2001) Gene regulation – a paradigm for precision. Science 293:1054–1055PubMedCrossRefGoogle Scholar
  97. Sundaresan V, Springer P, Volpe T et al (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev 9:1797–1810PubMedCrossRefGoogle Scholar
  98. Sunil Kumar GB, Ganapathi TR, Revathi CJ, Srinivas L, Bapat VA (2005) Expression of hepatitis B surface antigen in transgenic banana plants. Planta 222:484–493CrossRefGoogle Scholar
  99. Swennen R, Arinaitwe G, Cammue BPA et al (2003) Transgenic approaches for resistance to Mycosphaerellaleaf spot diseases in Musa spp. In: Mycosphaerella leaf spot diseases of bananas: present status and outlook. Proceedings of the 2nd international workshop on Mycosphaerella leaf spot diseases of bananas. L. Jacome, P. Lepoivre, D. Marin, R. Ortiz, R. Romero and J.V. Escalant, editors. San José, Costa Rica, 20–23 May 2002. INIBAP, Montpellier, France. pp. 209–238Google Scholar
  100. Tang Y, Kuang J, Wang F et al (2013) Molecular characterization of PR and WRKY genes during SA- and MeJA-induced resistance against Colletotrichum musae in banana fruit. Postharvest Biol Technol 79:62–68. doi: 10.1016/j.postharvbio.2013.01.004 CrossRefGoogle Scholar
  101. Teeri TH, Herrera-Estrella L, Depicker A, Van Montagu M, Palva ET (1986) Identification of plant promoters in situ by T-DNA-mediated transcriptional fusions to the npt-II gene. EMBO J 5:1755–1760PubMedPubMedCentralGoogle Scholar
  102. Thompson JF, Hayes LS, Lloyd DB (1991) Modulation of firefly luciferase stability and impact on studies of gene regulation. Gene 103:171–177PubMedCrossRefGoogle Scholar
  103. Topping JF, Wei WB, Lindsey K (1991) Functional tagging of regulatory elements in the plant genome. Development 112:1009–1019PubMedGoogle Scholar
  104. Van Leeuwen W, Hagendoorn MJM, Ruttink T et al (2000) The use of the luciferase reporter system for in planta gene expression studies. Plant Mol Biol Report 18:143a–143tCrossRefGoogle Scholar
  105. Vanhove AC, Vermaelen W, Swennen R, Carpentier SC (2015) A look behind the screens: characterization of the HSP70 family during osmotic stress in a non-model crop. J Proteomics 119:10–20. doi: 10.1016/j.jprot.2015.01.014 PubMedCrossRefGoogle Scholar
  106. Venter M, Botha FC (2004) Promoter analysis and transcription profiling: integration of genetic data enhances understanding of gene expression. Physiol Plant 120:74–83PubMedCrossRefGoogle Scholar
  107. Verkhusha VV, Kuznetsova IM, Stepanenko OV et al (2003) High stability of Discosoma DsRed as compared to Aequorea EGFP. Biochemistry 42:7879–7884PubMedCrossRefGoogle Scholar
  108. Vishnevetsky J, White TL Jr, Palmateer AJ et al (2011) Improved tolerance toward fungal diseases in transgenic Cavendish banana (Musa spp. AAA group) cv. Grand Nain. Transgenic Res 20:61–72. doi: 10.1007/s11248-010-9392-7 PubMedCrossRefGoogle Scholar
  109. Wang XL, Peng XX (2001a) Cloning of promoter of banana fruit-specific ACC synthase gene and primary study on its function. Chin J Biotechnol 17:293–296Google Scholar
  110. Wang XL, Peng XX (2001b) Cloning of promoter of banana fruit ripening-related ACO1 and primary study on its function. Chin J Biotechnol 17:428–431Google Scholar
  111. Wood KV (1995) Marker proteins for gene expression. Curr Opin Biotechnol 6:50–58PubMedCrossRefGoogle Scholar
  112. Wu CH, Madabusi L, Nishioka H et al (2001) Analysis of core promoter sequences located downstream from the TATA element in the hsp70 promoter from Drosophila melanogaster. Mol Cell Biol 21:1593–1602PubMedPubMedCentralCrossRefGoogle Scholar
  113. Xiao Y, Chen J, Kuang J et al (2013) Banana ethylene response factors are involved in fruit ripening through their interactions with ethylene biosynthesis genes. J Exp Bot 64(8):2499–2510. doi: 10.1093/jxb/ert108 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Yamamoto YY, Obokata J (2007) PPDB: a plant promoter database. Nucleic Acids Res 36:D977–D981PubMedPubMedCentralCrossRefGoogle Scholar
  115. Yamamoto YY, Ichida H, Matsui M et al (2007a) Identification of plant promoter constituents by analysis of local distribution of short sequences. BMC Genomics 8:67PubMedPubMedCentralCrossRefGoogle Scholar
  116. Yamamoto YY, Ichida H, Abe T et al (2007b) Differentiation of core promoter architecture between plants and mammals revealed by LDSS analysis. Nucleic Acids Res 35:6219–6226PubMedPubMedCentralCrossRefGoogle Scholar
  117. Yang IC, Iommarini JP, Becker DK et al (2003) A promoter derived from taro bacilliform badnavirus drives strong expression in transgenic banana and tobacco plants. Plant Cell Rep 21:1199–1206PubMedCrossRefGoogle Scholar
  118. Zhu Q, Dabi T, Lamb C (1995) TATA box and initiator functions in the accurate transcription of a plant minimal promoter in vitro. Plant Cell 7:1681–1689PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Singapore 2016

Authors and Affiliations

  • Efrén Santos
    • 1
    • 2
    Email author
  • Ricardo Pacheco
    • 2
  • Liliana Villao
    • 2
  • Luis Galarza
    • 1
    • 2
  • Daniel Ochoa
    • 3
  • Carlos Jordán
    • 3
  • José Flores
    • 1
    • 2
  1. 1.Escuela Superior Politécnica del Litoral, ESPOL, Facultad de Ciencias de la VidaGuayaquilEcuador
  2. 2.Escuela Superior Politécnica del Litoral, ESPOL, Centro de Investigaciones Biotecnológicas del Ecuador, CIBEGuayaquilEcuador
  3. 3.Escuela Superior Politécnica del Litoral, ESPOL, Centro de Visión y Robótica, Facultad de Ingeniería en Electricidad y ComputaciónGuayaquilEcuador

Personalised recommendations