biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 64:430-438, 2020 | DOI: 10.32615/bp.2020.036

Isolation and characterization of the promoter of SEPALLATA1-like gene from Platanus acerifolia

S.J. LU1,3, S.S. YI1,3, L. LIU1,4, M.Z. BAO1, G.F. LIU2,*
1 College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, P.R. China
2 Guangzhou Institute of Forestry and Landscape Architecture, Guangzhou, 510405, P.R. China
3 Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Danzhou, Hainan, 571737, P.R. China
4 District Management Committee of Xi'an North Railway Station, Xi'an, 710021, P.R. China

London plane (Platanus acerifolia Wild.) is a famous landscape plant because of its numerous desirable traits except the abundant pollens and seed hairs, which not only pollute the environment but also affect human health. To resolve these problems, we herein isolated and functionally analyzed the promoter of PlacSEP1.1, an orthologous gene of Arabidopsis SEPALLATA1, and investigated the potential usability for cell ablation strategies to engineer reproductive sterility in plants. A 2130 bp 5' upstream region of PlacSEP1.1 was isolated and termed pPlacSEP1.1. Putative motif detections show that there were several types of motifs in pPlacSEP1.1 including core promoter elements, tissue-specific expression regulatory elements, and some negative regulatory elements. β-Glucuronidase histochemical and quantitative assay showed that pPlacSEP1.1 of all deletions was active in all detected tissues except the shortest deletion D5 in roots. In order to test whether pPlacSEP1.1 could be used for London plane sterility breeding with a cytotoxic gene Barnase, the pPlacSEP1.1::Barnase and pPlacSEP1.1::Barnase-mic35S-Barstar vectors were constructed and transformed into tobacco. The pPlacSEP1.1::Barnase transgenic tobacco showed serious defects with respect to vegetative development and died within a couple of weeks after transplantation. On the other hand, most pPlacSEP1.1::Barnase-mic35S-Barstar transgenic tobacco showed normal vegetative growth and inflorescence, and flower development prevented phenotype.

Keywords: Agrobacterium mediated transformation, Arabidopsis thaliana, cytotoxic gene Barnase, London plane, Nicotiana tabacum, pollution, sterility.

Received: December 6, 2019; Revised: February 26, 2020; Accepted: March 2, 2020; Published online: June 1, 2020  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
LU, S.J., YI, S.S., LIU, L., BAO, M.Z., & LIU, G.F. (2020). Isolation and characterization of the promoter of SEPALLATA1-like gene from Platanus acerifolia. Biologia plantarum, 64, Article 430-438. https://doi.org/10.32615/bp.2020.036
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download fileLu6384 Suppl.pdf

    File size: 225.65 kB

    References

    1. Adam, H., Jouannic, S., Morcillo, F., Richaud, F., Duval, Y., Tregear, J.W.: MADS box genes in oil palm (Elaeis guineensis): patterns in the evolution of the SQUAMOSA, DEFICIENS, GLOBOSA, AGAMOUS, and SEPALLATA subfamilies. - J. mol. Evol. 62: 15-31, 2006. Go to original source...
    2. Asturias, J.A., Ibarrola, I., Bartolome, B., Ojeda, I., Malet, A., Martinez, A.: Purification and characterization of Pla a 1, a major allergen from Platanus acerifolia pollen. - Allergy 57: 221-227, 2002. Go to original source...
    3. Bate, N., Twel, D.: Functional architecture of a late pollen promoter: pollen-specific transcription is developmentally regulated by multiple stage-specific and co-dependent activator elements. - Plant mol. Biol. 37: 859-869, 1998. Go to original source...
    4. Beals, T.P., Goldberg, R.B.: A novel cell ablation strategy blocks tobacco anther dehiscence. - Plant Cell 9: 1527-1545, 1997. Go to original source...
    5. Block, M.D., Debrouwer, D., Moens, T.: The development of a nuclear male sterility system in wheat. Expression of the barnase gene under the control of tapetum specific promoters. - Theor. appl Genet. 95: 125-131, 1997. Go to original source...
    6. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal Biochem. 72: 248-254, 1976. Go to original source...
    7. Chang, Y.Y., Chiu, Y.F., Wu, J.W., Yang, C.H.: Four orchid (Oncidium Gower Ramsey) AP1/AGL9-like MADS box genes show novel expression patterns and cause different effects on floral transition and formation in Arabidopsis thaliana. - Plant Cell Physiol. 50: 1425-1438, 2009. Go to original source...
    8. Cheng, S.Y., Cheng, J.H., Xu, F., Ye, J.B., Wang, X.H.: Molecular cloning and expression analysis of a putative E class MADS-box gene, GbSEP, from Ginkgo biloba. - J. Anim. Plant Sci. 26: 253-260, 2016.
    9. Cui, R., Han, J., Zhao, S., Su, K., Wu, F., Du, X., Xu, Q., Chong, K., Theissen, G., Meng, Z.: Functional conservation and diversification of class E floral homeotic genes in rice (Oryza sativa). - Plant J. 61: 767-781, 2010. Go to original source...
    10. Denis, M., Delourme, R., Gourret, J.P., Mariani, C., Renard, M.: Expression of engineered nuclear male sterility in Brassica napus - genetics, morphology, cytology, and sensitivity to temperature. - Plant Physiol. 101: 1295-1304, 1993. Go to original source...
    11. Ditta, G., Pinyopich, A., Robles, P., Pelaz, S., Yanofsky, M.F.: The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. - Curr. Biol. 14: 1935-1940, 2004. Go to original source...
    12. Elorriaga, E., Meilan, R., Ma, C., Skinner, J.S., Etherington, E., Brunner,A., Strauss, S.H.: A tapetal ablation transgene induces stable male sterility and slows field growth in Populus. - Tree Genet. Genomes 10: 1583-1593, 2014. Go to original source...
    13. Enrique, E., Cistero-Bahima, A., Bartolome, B., Alonso, R., San Miguel-Moncin, M.M., Bartra, J., Martinez, A.: Platanus acerifolia pollinosis and food allergy. - Allergy 57: 351-356, 2002. Go to original source...
    14. Ferrario, S., Immink, R.G., Shchennikova, A., Busscher-Lange, J., Angenent, G.C.: The MADS box gene FBP2 is required for SEPALLATA function in petunia. - Plant Cell 15: 914-925, 2003. Go to original source...
    15. Flanagan, C.A., Ma, H.: Spatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant Arabidopsis flowers. - Plant mol. Biol. 26: 581-595, 1994. Go to original source...
    16. Garcia-Sogo, B., Pineda, B., Castelblanque, L., Anton, T., Medina, M., Roque, E., Torresi, C., Beltran, J.P., Moreno, V., Canas, L.A.: Efficient transformation of Kalanchoe blossfeldiana and production of male-sterile plants by engineered anther ablation. - Plant Cell Rep. 29: 61-77, 2010. Go to original source...
    17. Garcia-Sogo, B., Pineda, B., Roque, E., Anton, T., Atares, A., Borja, M., Beltran, J.P., Moreno, V., Canas, L.A.: Production of engineered long-life and male sterile Pelargonium plants. - BMC Plant Biol. 12: 156, 2012. Go to original source...
    18. Goldman, M.H., Goldberg, R.B., Mariani, C.: Female sterile tobacco plants are produced by stigma-specific cell ablation. - EMBO J. 13: 2976-2984, 1994. Go to original source...
    19. Hartley, R.W.: Barnase and barstar: expression of its cloned inhibitor permits expression of a cloned ribonuclease. - J. mol. Biol. 202: 913-915, 1988. Go to original source...
    20. Hernandez-Garcia, C.M., Finer, J.J.: Identification and validation of promoters and cis-acting regulatory elements. - Plant Sci. 217-218: 109-119, 2014. Go to original source...
    21. Higo, K., Ugawa, Y., Iwamoto, M., Korenaga, T.: Plant cis-acting regulatory DNA elements (PLACE) database: 1999. - Nucl. Acid. Res. 27: 297-300, 1999. Go to original source...
    22. Horsch, R.B., Rogers, S.G., Fraley, R.T.: Transgenic plants. - Cold Spring Harbour Symp. Quant. Biol. 50: 433-437, 1985. Go to original source...
    23. Huang H., Tudor M., Weiss C.A., Hu Y., Ma H.: The Arabidopsis MADS-box gene AGL3 is widely expressed and encodes a sequence-specific DNA-binding protein. - Plant mol. Biol. 28: 549-567, 1995. Go to original source...
    24. Ireland, H.S., Yao, J.L., Tomes, S., Sutherland, P.W., Nieuwenhuizen, N., Gunaseelan, K., Winz, R.A., David, K.M., Schaffer, R.J.: Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. - Plant J. 73: 1044-1056, 2013. Go to original source...
    25. Jang, S., An, K., Lee, S., An, G.: Characterization of tobacco MADS-box genes involved in floral initiation. - Plant Cell Physiol. 43: 230-238, 2002. Go to original source...
    26. Jefferson, R.A., Kavanagh, T.A., Bevan, M.W.: GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. - EMBO J. 6: 3901-3907, 1987. Go to original source...
    27. Krizek, B.A., Fletcher, J.C.: Molecular mechanisms of flower development: an armchair guide. - Nat. Rev. Genet. 6: 688-698, 2005. Go to original source...
    28. Lännenpää, M., Hassinen, M., Ranki, A., Hölttä-Vuori, M., Lemmetyine, J., Keinonen, K., Sopanen, T.: Prevention of flower development in birch and other plants using a BpFULL1::BARNASE construct. - Plant Cell Rep. 24: 69-78, 2005. Go to original source...
    29. Lee, J., Oh, M., Park, H., Lee, I.: SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. - Plant J. 55: 832-843, 2008. Go to original source...
    30. Lee, Y.H., Chung, K.H., Kim, H.U., Jin, Y.M., Kim, H.I., Park, B.S.: Induction of male sterile cabbage using a tapetum-specific promoter from Brassica campestris L. ssp. pekinensis. - Plant Cell Rep. 22: 268-273, 2003. Go to original source...
    31. Lemmetyinen, J., Keinonen, K., Sopanen, T.: Prevention of the flowering of a tree, silver birch. - Mol. Breed. 13: 243-249, 2004. Go to original source...
    32. Lescot, M., Dehais, P., Thijs, G., Marchal, K., Moreau, Y., Van de Peer, Y., Rouze, P., Rombauts, S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. - Nucl. Acids Res. 30: 325-327, 2002. Go to original source...
    33. Li, Z.N., Fang, F., Liu, G.F., Bao, M.Z.: Stable Agrobacterium-mediated genetic transformation of London plane tree (Platanus acerifolia Willd.). - Plant Cell Rep. 26: 641-650, 2007. Go to original source...
    34. Liu, Y.G., Huang, N.: Efficient amplification of insert end sequences from bacterial artificial chromosome clones by thermal asymmetric interlaced PCR. - Plant mol. Biol. Rep. 16: 175-181, 1998. Go to original source...
    35. Liu, Y.G., Mitsukawa, N., Oosumi, T., Whittier ,R.F.: Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. - Plant J. 8: 457-463, 1995. Go to original source...
    36. Lu, S.J., Li, Z.N., Zhang, J.Q., Yi, S.S., Liu, L., Bao, M.Z., Liu, G.F.: Isolation and expression analysis of a LEAFY/FLORICAULA homolog and its promoter from London plane (Platanus acerifolia Willd.). - Plant Cell Rep. 31: 1851-1865, 2012. Go to original source...
    37. Ma, H., Yanofsky, M.F., Meyerowitz, E.M.: AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. - Genes Dev. 5: 484-495, 1991. Go to original source...
    38. Mahmood, T., Zar, T., Naqvi, S.M.S.: Multiple pulses improve electroporation efficiency in Agrobacterium tumefaciens. - Electron J. Biotechn. 11: 1-4, 2008. Go to original source...
    39. Mandel, M., Yanofsky, M.F.: The Arabidopsis AGL9 MADS box gene is expressed in young flower primordia. - Sex Plant Reprod. 11: 22-28, 1998. Go to original source...
    40. Mariani, C., Beuckeleer, M.D., Truettner, J., Leemans, J., Goldberg, R.B.: Induction of male sterility in plants by a chimaeric ribonuclease gene. - Nature 347: 737-741, 1990. Go to original source...
    41. Mariani, C., Gossele, V., Beuckeleer, M.D., Block, M.D., Goldberg, R.B., Greef, W.D., Leemans, J.: A chimaeric ribonuclease-inhibitor gene restores fertility to male sterile plants. - Nature 357: 384-387, 1992. Go to original source...
    42. Matsubara, K., Shimamura, K., Kodama, H., Kokubun, H., Watanabe, H., Basualdo, I.L., Ando, T.: Green corolla segments in a wild Petunia species caused by a mutation in FBP2, a SEPALLATA-like MADS box gene. - Planta 228: 401-409, 2008. Go to original source...
    43. Matsunaga, S., Uchida, W., Kejnovsky, E., Isono, E., Moneger, F., Vyskot, B., Kawano, S.: Characterization of two SEPALLATA MADS-box genes from the dioecious plant Silene latifolia. - Sex Plant Reprod. 17: 189-193, 2004. Go to original source...
    44. Mena, M., Vicente-Carbajosa, J., Schmidt, R.J., Carbonero, P.: An endosperm-specific DOF protein from barley, highly conserved in wheat, binds to and activates transcription from the prolamin-box of a native B-hordein promoter in barley endosperm. - Plant J. 16: 53-62, 1998. Go to original source...
    45. Murashige, T., Skoog, F.: A revised medium for rapid growth and bio assays with tobacco tissue cultures. - Physiol Plant. 15: 473-497, 1962. Go to original source...
    46. Pan, Z.J., Chen, Y.Y., Du, J.S., Chen, Y.Y., Chung, M.C., Tsai, W.C., Wang, C.N., Chen, H.H.: Flower development of Phalaenopsis orchid involves functionally divergent SEPALLATA-like genes. - New Phytol. 202: 1024-1042, 2014. Go to original source...
    47. Pelaz, S., Ditta, G.S., Baumann, E., Wisman, E., Yanofsky, M.F.: B and C floral organ identity functions require SEPALLATA MADS-box genes. - Nature 405: 200-203, 2000. Go to original source...
    48. Riechmann, J.L., Krizek, B.A., Meyerowitz, E.M.: Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. - Proc. nat. Acad. Sci. USA 93: 4793-4798, 1996. Go to original source...
    49. Riechmann, J.L., Meyerowitz, E.M.: Determination of floral organ identity by Arabidopsis MADS domain homeotic proteins AP1, AP3, PI, and AG is independent of their DNA-binding specificity. - Mol. Biol. Cell 8: 1243-1259, 1997. Go to original source...
    50. Rogers, H.J., Bate, N., Combe, J., Sullivan, J., Sweetman, J., Swan, C., Lonsdale, D.M., Twell, D.: Functional analysis of cis-regulatory elements within the promoter of the tobacco late pollen gene g10. - Plant mol. Biol. 45: 577-585, 2001. Go to original source...
    51. Roque, E., Gomez, M.D., Ellul, P., Wallbraun, M., Madueno, F., Beltran, J.P., Canas, L.A.: The PsEND1 promoter: a novel tool to produce genetically engineered male-sterile plants by early anther ablation. - Plant Cell Rep. 26: 313-325, 2007. Go to original source...
    52. Savidge, B., Rounsley, S.D., Yanofsky, M.F.: Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. - Plant Cell 7: 721-733, 1995. Go to original source...
    53. Skinner, J.S., Meilan, R., Brunner, A.M., Strauss, S.H.: Options for genetic engineering of floral sterility in forest trees. - Mol. Biol. Woody Plants 2000: 135-153, 2000. Go to original source...
    54. Sun, W., Huang, W., Li, Z., Song, C., Liu, D., Liu, Y., Hayward, A., Liu, Y., Huang, H., Wang, Y.: Functional and evolutionary analysis of the AP1/SEP/AGL6 superclade of MADS-box genes in the basal eudicot Epimedium sagittatum. - Ann. Bot. 113: 653-668, 2014. Go to original source...
    55. Tani, E., Polidoros, A.N., Flemetakis, E., Stedel, C., Kalloniati, C., Demetriou, K., Katinakis, P., Tsaftaris A.S.: Characterization and expression analysis of AGAMOUS-like, SEEDSTICK-like, and SEPALLATA-like MADS-box genes in peach (Prunus persica) fruit. - Plant Physiol. Biochem. 47: 690-700, 2009. Go to original source...
    56. Theissen, G.: Development of floral organ identity: stories from the MADS house. - Curr. Opin. Plant Biol. 4: 75-85, 2001. Go to original source...
    57. Tzeng, T.Y., Hsiao, C.C., Chi, P.J., Yang, C.H.: Two lily SEPALLATA-like genes cause different effects on floral formation and floral transition in Arabidopsis. - Plant Physiol. 133: 1091-1101, 2003. Go to original source...
    58. Uimari, A., Kotilainen, M., Elomaa, P., Yu, D., Albert, V.A., Teeri, T.H.: Integration of reproductive meristem fates by a SEPALLATA-like MADS-box gene. - Proc. nat. Acad. Sci. USA 101: 15817-15822, 2004. Go to original source...
    59. Van den Bussche, M., Zethof, J., Souer, E., Koes, R., Tornielli, G.B., Pezzotti, M., Ferrario, S., Angenent, G.C., Gerats, T.: Toward the analysis of the petunia MADS box gene family by reverse and forward transposon insertion mutagenesis approaches: B, C, and D floral organ identity functions require SEPALLATA-like MADS box genes in petunia. - Plant Cell 15: 2680-2693, 2003. Go to original source...
    60. Washida, H., Wu, C.Y., Suzuki, A., Yamanouchi, U., Akihama, T., Harada, K., Takaiwa, F.: Identification of cis-regulatory elements required for endosperm expression of the rice storage protein glutelin gene GluB-1. - Plant mol. Biol. 40: 1-12, 1999. Go to original source...
    61. Wu, C., Washida, H., Onodera, Y., Harada, K., Takaiwa, F.: Quantitative nature of the Prolamin-box, ACGT and AACA motifs in a rice glutelin gene promoter: minimal cis-element requirements for endosperm-specific gene expression. - Plant J. 23: 415-421, 2000. Go to original source...
    62. Xu, Y., Zhang, L., Xie, H., Zhang, Y.Q., Oliveira, M.M., Ma, R.C.: Expression analysis and genetic mapping of three SEPALLATA-like genes from peach (Prunus persica (L.) Batsch). - Tree Genet. Genomes 4: 693-703, 2008. Go to original source...
    63. Yoshino, M., Nagamatsu, A., Tsutsumi, K., Kanazawa, A.: The regulatory function of the upstream sequence of the beta-conglycinin alpha subunit gene in seed-specific transcription is associated with the presence of the RY sequence. - Genes Genet. Syst. 81: 135-141, 2006. Go to original source...
    64. Zhang, C., Norris-Caneda, K.H., Rottmann, W.H., Gulledge, J.E., Chang, S., Kwan, B.Y., Thomas, A.M., Mandel, L.C., Kothera, R.T., Victor, A.D., Pearson, L., Hinchee, M.A.W.: Control of pollen-mediated gene flow in transgenic trees. - Plant Physiol. 159: 1319-1334, 2012. Go to original source...
    65. Zhang, S.S., Lu, S.J., Yi, S.S., Han, H.J., Liu, L., Zhang, J.Q., Bao, M.Z., Liu, G.F.: Functional conservation and divergence of five SEPALLATA-like genes from a basal eudicot tree, Platanus acerifolia. - Planta 245: 439-457, 2017. Go to original source...

    Return to the content