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

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Biologia Plantarum

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.

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Abbreviations

ELISA:

enzyme-linked immunosorbent assay

GA:

gibberellin

PAC:

paclobutrazol

UPS:

ubiquitin-26S proteasome system

WT:

wild-type

References

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Callis, J., Vierstra, R.D.: Protein degradation in signaling. — Curr. Opin. Plant Biol. 3: 381–386, 2000.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Dellaporta, S.L., Wood, J., Hicks, J.B.: A plant DNA minipreparation: version II. — Plant mol. Biol. Rep. 1: 19–21, 1983.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doherty, F., Dawson, S., Mayer, R.: The ubiquitin-proteasome pathway of intracellular proteolysis. — Essays Biochem. 38: 51–63, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Fleet, C.M., Sun, T.P.: A DELLAcate balance: the role of gibberellin in plant morphogenesis. — Curr. Opin. Plant Biol. 8: 77–85, 2005.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Harberd, N.P.: Relieving DELLA restraint. — Science 299: 1853–1854, 2003.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Hooley, R.: Gibberellins: perception, transduction and responses. — Plant mol. Biol. 26: 1529–1555, 1994.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Kepinski, S., Leyser, O.: The Arabidopsis F-box protein TIR1 is an auxin receptor. — Nature 435: 446–451, 2005.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moon, J., Parry, G., Estelle, M.: The ubiquitin-proteasome pathway and plant development. — Plant Cell 16: 3181–3195, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakayama, K.I., Nakayama, K.: Ubiquitin ligases: cell-cycle control and cancer. — Nat. Rev. Cancer 6: 369–381, 2006.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petroski, M.D., Deshaies, R.J.: Function and regulation of cullin-RING ubiquitin ligases. — Nat. Rev. mol. cell. Biol. 6: 9–20, 2005.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santner, A., Estelle, M.: Recent advances and emerging trends in plant hormone signalling. — Nature 459: 1071–1078, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Santner, A., Estelle, M.: The ubiquitin-proteasome system regulates plant hormone signaling. — Plant J. 61: 1029–1040, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Sun, T.P., Gubler, F.: Molecular mechanism of gibberellin signaling in plants. — Annu. Rev. Plant Biol. 55: 197–223, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Thomas, S.G., Rieu, I., Steber, C.M.: Gibberellin metabolism and signaling. — Vitamins Hormones 72: 289–338, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Vierstra, R.D.: The ubiquitin-26S proteasome system at the nexus of plant biology. — Nat. Rev. mol. cell. Biol. 10: 385–397, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Wang, F., Deng, X.W.: Plant ubiquitin-proteasome pathway and its role in gibberellin signaling. — Cell Res. 21: 1286–1294, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson, K.D.: Ubiquitination and deubiquitination: targeting of proteins for degradation by the proteasome. — Semin. cell. dev. Biol. 11: 141–148, 2000.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi, S.: Gibberellin metabolism and its regulation. — Annu. Rev. Plant Biol. 59: 225–251, 2008.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to W. Wang.

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Acknowledgements: This study was supported by the National Natural Science Foundation of China (No. 31370304), by the Natural Science Foundation of Shandong Province, China (No. ZR2015CL037), and by the Opening Foundation of State Key Laboratory of Crop Biology (2013KF01). The first two authors contributed equally to this paper.

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Yin, S., Zhou, S., Kong, X. et al. Altered gibberellin content affects growth and development in transgenic tobacco lines overexpressing a wheat gene encoding F-box protein. Biol Plant 61, 349–358 (2017). https://doi.org/10.1007/s10535-017-0707-x

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  • DOI: https://doi.org/10.1007/s10535-017-0707-x

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