Advertisement

Biologia Plantarum

, Volume 61, Issue 2, pp 349–358 | Cite as

Altered gibberellin content affects growth and development in transgenic tobacco lines overexpressing a wheat gene encoding F-box protein

  • S. Yin
  • S. Zhou
  • X. Kong
  • Y. Han
  • W. WangEmail author
Original Paper

Abstract

In a previous study, we have identified and characterized gene from wheat (Triticum aestivum L.) encoding F-box protein and named it TaFBA. In this paper, transgenic tobacco (Nicotiana tabacum L.) plants overexpressing TaFBA1 displayed accelerated growth early, but the rate slowed gradually at later stages of growth, and the mature transgenic plants were even shorter in stature and flowered later than did the wild type (WT). Treatment with gibberellin (GA) conferred an accelerated growth rate to the transgenic tobacco plants at later stages, similar to that of WT, whereas growth was inhibited more seriously in WT than in transgenic tobacco when plants were treated with a GA biosynthesis inhibitor. The content of GA in transgenic tobacco plants was higher at early developmental stages, but it was lower at later growth stages than in WT. Some GA biosynthesis genes were down regulated, which was accompanied with elevated expression of a GA catabolism gene. Thus, our results suggest that TaFBA1 is possibly involved in the regulation of plant growth and development, and that it may be related to the production, metabolism, and proper function of GA.

Additional key words

ELISA Nicotiana tabacum paclobutrazol RT-qPCR Triticum aestivum 

Abbreviations

ELISA

enzyme-linked immunosorbent assay

GA

gibberellin

PAC

paclobutrazol

UPS

ubiquitin-26S proteasome system

WT

wild-type

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

10535_2017_707_MOESM1_ESM.pdf (69 kb)
Supplementary material, approximately 70 KB.

References

  1. Calderon-Villalobos, L.I.A., Nill, C., Marrocco, K., Kretsch, T., Schwechheimer, C.: The evolutionarily conserved Arabidopsis thaliana F-box protein AtFBP7 is required for efficient translation during temperature stress. — Gene 392: 106–116, 2007.CrossRefPubMedGoogle Scholar
  2. Callis, J., Vierstra, R.D.: Protein degradation in signaling. — Curr. Opin. Plant Biol. 3: 381–386, 2000.CrossRefPubMedGoogle Scholar
  3. Cao, D., Cheng, H., Wu, W., Soo, H.M., Peng, J.: Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. — Plant Physiol. 142: 509–525, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chandler, P.M., Marion-Poll, A., Ellis, M., Gubler, F.: Mutants at the Slender 1 locus of barley cv Himalaya. Molecular and physiological characterization. — Plant Physiol. 129: 181–190, 2002.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Coates, J.C., Laplaze, L., Haseloff, J.: Armadillo-related proteins promote lateral root development in Arabidopsis. — Proc. nat. Acad. Sci. USA 103: 1621–1626, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Craig, K.L., Tyers, M.: The F-box: a new motif for ubiquitindependent proteolysis in cell-cycle regulation and signal transduction. — Progr. Biophys. mol. Biol. 72: 299–328, 1999.CrossRefGoogle Scholar
  7. Dellaporta, S.L., Wood, J., Hicks, J.B.: A plant DNA minipreparation: version II. — Plant mol. Biol. Rep. 1: 19–21, 1983.CrossRefGoogle Scholar
  8. Dill, A., Thomas, S.G., Hu, J., Steber, C.M., Sun, T.P.: The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. — Plant Cell 16: 1392–1405, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Doherty, F., Dawson, S., Mayer, R.: The ubiquitin-proteasome pathway of intracellular proteolysis. — Essays Biochem. 38: 51–63, 2002.CrossRefPubMedGoogle Scholar
  10. Fleet, C.M., Sun, T.P.: A DELLAcate balance: the role of gibberellin in plant morphogenesis. — Curr. Opin. Plant Biol. 8: 77–85, 2005.CrossRefPubMedGoogle Scholar
  11. Gagne, J.M., Smalle, J., Gingerich, D.J., Walker, J.M., Yoo, S.D., Yanagisawa, S., Vierstra, R.D.: Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. — Proc. nat. Acad. Sci. USA 101: 6803–6808, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gallego-Giraldo, L., Ubeda-Tomas, S., Gisbert, C., Garcia-Martinez, J.L., Moritz, T., Lopez-Diaz, I.: Gibberellin homeostasis in tobacco is regulated by gibberellin metabolism genes with different gibberellin sensitivity. — Plant Cell Physiol. 49: 679–690, 2008.CrossRefPubMedGoogle Scholar
  13. Gray, W.M., Kepinski, S., Rouse, D., Leyser, O., Estelle, M.: Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. — Nature 414: 271–276, 2001.CrossRefPubMedGoogle Scholar
  14. Harberd, N.P.: Relieving DELLA restraint. — Science 299: 1853–1854, 2003.CrossRefPubMedGoogle Scholar
  15. Hartweck, L.M., Olszewski, N.E.: Rice GIBBERELLIN INSENSITIVE DWARF1 is a gibberellin receptor that illuminates and raises questions about GA signaling. — Plant Cell 18: 278–282, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ho, M., Ou, C., Chan, Y.R., Chien, C.T., Pi, H.: The utility F-box for protein destruction. — Cell. Mol. Life Sci. 65: 1977–2000, 2008.CrossRefPubMedGoogle Scholar
  17. Hoagland, D.R., Arnon, D.I.: The water-culture method for growing plants without soil. - California Agricultural Experiment Station Circular. 2nd Ed. Pp. 347, 1950.Google Scholar
  18. Hooley, R.: Gibberellins: perception, transduction and responses. — Plant mol. Biol. 26: 1529–1555, 1994.CrossRefPubMedGoogle Scholar
  19. Hu, Z., Keceli, M.A., Piisilä, M., Li, J., Survila, M., Heino, P., Brader, G., Palva, E.T., Li, J.: F-box protein AFB4 plays a crucial role in plant growth, development and innate immunity. — Cell Res. 22: 777–781, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Jain, M., Nijhawan, A., Arora, R., Agarwal, P., Ray, S., Sharma, P., Kapoor, S., Tyagi, A.K., Khurana, J.P.: F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. — Plant Physiol. 143: 1467–1483, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Jia, Y., Gu, H., Wang, X., Chen, Q., Shi, S., Zhang, J., Ma, L., Zhang, H., Ma, H.: Molecular cloning and characterization of an F-box family gene CarF-box1 from chickpea (Cicer arietinum L.). — Mol. Biol. Rep. 39: 2337–2345, 2012.CrossRefPubMedGoogle Scholar
  22. Kepinski, S., Leyser, O.: The Arabidopsis F-box protein TIR1 is an auxin receptor. — Nature 435: 446–451, 2005.CrossRefPubMedGoogle Scholar
  23. McGinnis, K.M., Thomas, S.G., Soule, J.D., Strader, L.C., Zale, J.M., Sun, T.P., Steber, C.M.: The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. — Plant Cell 15: 1120–1130, 2003.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Moon, J., Parry, G., Estelle, M.: The ubiquitin-proteasome pathway and plant development. — Plant Cell 16: 3181–3195, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Nakayama, K.I., Nakayama, K.: Ubiquitin ligases: cell-cycle control and cancer. — Nat. Rev. Cancer 6: 369–381, 2006.CrossRefPubMedGoogle Scholar
  26. Ni, W., Xie, D., Hobbie, L., Feng, B., Zhao, D., Akkara, J., Ma, H.: Regulation of flower development in Arabidopsis by SCF complexes. — Plant Physiol. 134: 1574–1585, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Petroski, M.D., Deshaies, R.J.: Function and regulation of cullin-RING ubiquitin ligases. — Nat. Rev. mol. cell. Biol. 6: 9–20, 2005.CrossRefPubMedGoogle Scholar
  28. Potuschak, T., Lechner, E., Parmentier, Y., Yanagisawa, S., Grava, S., Koncz, C., Genschik, P.: EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F-box proteins: EBF1 and EBF2. — Cell 115: 679–689, 2003.CrossRefPubMedGoogle Scholar
  29. Richards, D.E., King, K.E., Ait-ali, T., Harberd, N.P.: How gibberellin regulates plant growth and development: a molecular genetic analysis of gibberellin signaling. — Annu. Rev. Plant Biol. 52: 67–88, 2001.CrossRefGoogle Scholar
  30. Ruegger, M., Dewey, E., Gray, W.M., Hobbie, L., Turner, J., Estelle, M.: The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast Grr1p. — Genes Dev. 12: 198–207, 1998.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Santner, A., Estelle, M.: Recent advances and emerging trends in plant hormone signalling. — Nature 459: 1071–1078, 2009.CrossRefPubMedGoogle Scholar
  32. Santner, A., Estelle, M.: The ubiquitin-proteasome system regulates plant hormone signaling. — Plant J. 61: 1029–1040, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Sasaki, A., Itoh, H., Gomi, K., Ueguchi-Tanaka, M., Ishiyama, K., Kobayashi, M., Jeong, D.H., An, G., Kitano, H., Ashikari, M.: Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. — Science 299: 1896–1898, 2003.CrossRefPubMedGoogle Scholar
  34. Souer, E., Rebocho, A.B., Bliek, M., Kusters, E., de Bruin, R.A., Koes, R.: Patterning of inflorescences and flowers by the F-box protein DOUBLE TOP and the LEAFY homolog ABERRANT LEAF AND FLOWER of petunia. — Plant Cell 20: 2033–2048, 2008.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Steber, C.M., Cooney, S.E., McCourt, P.: Isolation of the GAresponse mutant sly1 as a suppressor of ABI 1-1 in Arabidopsis thaliana. — Genetics 149: 509–521, 1998.PubMedPubMedCentralGoogle Scholar
  36. Strader, L.C., Ritchie, S., Soule, J.D., McGinnis, K.M., Steber, C.M.: Recessive-interfering mutations in the gibberellin signaling gene SLEEPY1 are rescued by overexpression of its homologue, SNEEZY. — Proc. Natl. Acad. Sci. USA. 101: 12771–12776, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Sullivan, J.A., Shirasu, K., Deng, X.W.: The diverse roles of ubiquitin and the 26S proteasome in the life of plants. — Nat. Rev. Genet. 4: 948–958, 2003.CrossRefPubMedGoogle Scholar
  38. Sun, T.P., Gubler, F.: Molecular mechanism of gibberellin signaling in plants. — Annu. Rev. Plant Biol. 55: 197–223, 2004.CrossRefPubMedGoogle Scholar
  39. Thomas, S.G., Rieu, I., Steber, C.M.: Gibberellin metabolism and signaling. — Vitamins Hormones 72: 289–338, 2005.CrossRefPubMedGoogle Scholar
  40. Vierstra, R.D.: The ubiquitin-26S proteasome system at the nexus of plant biology. — Nat. Rev. mol. cell. Biol. 10: 385–397, 2009.CrossRefPubMedGoogle Scholar
  41. Wang, F., Deng, X.W.: Plant ubiquitin-proteasome pathway and its role in gibberellin signaling. — Cell Res. 21: 1286–1294, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Wang, G.K., Zhang, M., Gong, J.F., Guo, Q.F., Feng, Y.N., Wang, W.: Increased gibberellin contents contribute to accelerated growth and development of transgenic tobacco overexpressing a wheat ubiquitin gene. — Plant Cell Rep. 31: 2215–2227, 2012.CrossRefPubMedGoogle Scholar
  43. Wilkinson, K.D.: Ubiquitination and deubiquitination: targeting of proteins for degradation by the proteasome. — Semin. cell. dev. Biol. 11: 141–148, 2000.CrossRefPubMedGoogle Scholar
  44. Willige, B.C., Ghosh, S., Nill, C., Zourelidou, M., Dohmann, E.M., Maier, A., Schwechheimer, C.: The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. — Plant Cell 19: 1209–1220, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Yamaguchi, S.: Gibberellin metabolism and its regulation. — Annu. Rev. Plant Biol. 59: 225–251, 2008.CrossRefPubMedGoogle Scholar
  46. Yang, J., Zhang, J., Wang, Z., Zhu, Q., Wang, W.: Hormonal changes in the grains of rice subjected to water stress during grain filling. — Plant Physiol. 127: 315–323, 2001.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Zentella, R., Zhang, Z.L., Park, M., Thomas, S.G., Endo, A., Murase, K., Fleet, C.M., Jikumaru, Y., Nambara, E., Kamiya, Y., Sun, T.P.: Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. — Plant Cell 19: 3037–3057, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Zhou, S.M., Sun, X.D., Yin, S.H., Kong, X.Z., Zhou, S., Xu, Y., Luo, Y., Wang, W.: The role of the F-box gene TaFBA1 from wheat (T. aestivum L.) in drought tolerance. — Plant Physiol. Biochem. 84: 213–223, 2014.CrossRefPubMedGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2017

Authors and Affiliations

  1. 1.State Key Laboratory of Crop Biology, Shandong Key Laboratory of Crop Biology, College of Life ScienceShandong Agricultural UniversityTai’an, ShandongP.R. China

Personalised recommendations