Abstract
Fruit growth is a coordinated, complex interaction of cell division, differentiation and expansion. Gibberellin (GA) involvement in the reproductive events is an important aspect of GA effects. Perennial fruit-trees such as plum (Prunus salicina L.) have distinct features that are economically important and provide opportunities to dissect specific GA mechanisms. Currently, very little is known on the molecular mechanism(s) mediating GA effects on fruit development. Determination of bioactive GA content during plum fruit ontogeny revealed that GA1 and GA4 are critical for fruit growth and development. Further, characterization of several genes involved in GA-signalling showed that their transcriptional regulation are generally GA-dependent, confirming their involvement in GA-signalling. Based on these results, a model is presented elucidating how the potential association between GA and other hormones may contribute to fruit development. PslGID1 proteins structure, Y2H and BiFC assays indicated that plum GA-receptors can form a complex with AtDELLA-repressors in a GA-dependent manner. Moreover, phenotypical-, molecular- and GA-analyses of various Arabidopsis backgrounds ectopically expressing PslGID1 sequences provide evidence on their role as active GA-signalling components that mediate GA-responsiveness. Our findings support the critical contribution of GA alone or in association with other hormones in mediating plum fruit growth and development.
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References
Achard P, Vriezen WH, Van Der Straeten D, Harberd NP (2003) Ethylene regulates Arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15:2816–2825
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Ariizumi T, Murase K, Sun TP, Steber CM (2008) Proteolysis-independent downregulation of DELLA repression in Arabidopsis by the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1. Plant Cell 20:2447–2459
Augustí M, Almela V, Andreu I, Juan M, Zacarias L (1999) Synthetic auxin 3,5,6-TPA promotes fruit development and climacteric in Prunus persica L. Batsch. J Hortic Sci Biotech 74:556–560
Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 98:10037–10041
Biemelt S, Tschiersch H, Sonnewald U (2004) Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol 135:254–265
Bjorklund S, Antti H, Uddestrand I, Moritz T, Sundberg B (2007) Cross-talk between gibberellin and auxin in development of Populus wood: gibberellin stimulates polar auxin transport and has a common transcriptome with auxin. Plant J 52:499–511
Bukovac MJ, Nakagawa S (1967) Comparative potency of gibberellins in inducing parthenocarpic fruit growth in Malus sylvestris Mill. Experientia 23:865
Bukvoac MJ (1963) Induction of parthenocarpic growth of apple fruits with gibberellins A3 and A4. Bot Gaz 124:191–195
Bukvoac MJ, Yuda E (1979) Endogenous plant growth substances in developing fruit of Prunus cerasus L. Plant Physiol 63:129–132
Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D et al (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064
Crane J (1964) Growth substances in fruit setting and development. Annu Rev Plant Physiol 15:303–326
Csukasi F, Osorio S, Gutierrez JR, Kitamura J, Giavalisco P, Nakajima M et al (2011) Gibberellin biosynthesis and signalling during development of the strawberry receptacle. New Phytol 191:376–390
de Jong M, Mariani C, Vriezen WH (2009) The role of auxin and gibberellin in tomato fruit set. J Exp Bot 60:1523–1532
Dill A, Sun TP (2001) Synergistic de-repression of gibberellin signalling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159:777–785
Dunberg A, Odén PC (1983) Gibberellins and conifers. In: Crozier A (ed) The biochemistry and physiology of gibberellins. Praeger, New York, pp 221–295
El-Sharkawy I, Kim WS, El-Kereamy A, Jayasankar S, Svircev AM, Brown DCW (2007) Isolation and characterization of four ethylene signal transduction elements in plums (Prunus salicina L.). J Exp Bot 58:3631–3643
El-Sharkawy I, Kim WS, Jayasankar S, Svircev AM, Brown DCW (2008) Differential regulation of four members of ACC synthase gene family in plum. J Exp Bot 59:2009–2027
El-Sharkawy I, Sherif S, Mila I, Bouzayen M, Jayasankar S (2009) Molecular characterization of seven genes encoding ethylene-responsive transcriptional factors during plum fruit development and ripening. J Exp Bot 60:907–922
El-Sharkawy I, Mila I, Bouzayen M, Jayasankar S (2010) Regulation of two germin-like protein genes during plum fruit development. J Exp Bot 61:1761–1770
El-Sharkawy I, Sherif S, Mahboob A, Abubaker K, Bouzayen M, Jayasankar S (2012a) Expression of auxin-binding protein1 during plum fruit ontogeny supports the potential role of auxin in initiating and enhancing climacteric ripening. Plant Cell Rep 31:1911–1921
El-Sharkawy I, El Kayal W, Prasath D, Fernández H, Bouzayen M, Svircev AM et al (2012b) Identification and genetic characterization of a gibberellin 2-oxidase gene that controls tree stature and reproductive growth in plum. J Exp Bot 63:1225–1239
Fleet CM, Sun TP (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8:77–85
Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451
Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ et al (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18:3399–3414
Harberd NP, Belfield E, Yasumura Y (2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an “Inhibitor of an inhibitor” enables flexible response to fluctuating environments. Plant Cell 21:1328–1339
Hedden P (2008) Plant biology: gibberellins close the lid. Nature 456:455–456
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300
Jackson DI (1968) Gibberellin in the growth of peach and apricot fruits. Aust J Biol Sci 21:209–215
Lee LY, Fang MJ, Kuang LY, Gelvin SB (2008) Vectors for multi-color bimolecular fluorescence complementation to investigate protein–protein interactions in living plant cells. Plant Meth 4:24
Lodhi F, Bradley MV, Crane JC (1969) Auxins and gibberellin-like substances in parthenocarpic and non-parthenocarpic syconia of Ficus carica L., cv. King. Plant Physiol 44:555–561
Mesejo C, Yuste R, Martínez-Fuentes A, Reig C, Iglesias DJ, Primo-Millo E, Agustí M (2013) Self-pollination and parthenocarpic ability in developing ovaries of self-incompatible Clementine mandarins (Citrus clementina). Physiol Plant 148:87–96
Miller AN, Walsh CS, Cohen JD (1987) Measurement of indole-3-acetic acid in peach fruits (Prunus persica L. Batsch cv. Redhaven) during development. Plant Physiol 84:491–494
Nakajima M, Shimada A, Takashi Y, Kim YC, Park SH, Ueguchi-Tanaka M et al (2006) Identification and characterization of Arabidopsis gibberellin receptors. Plant J 46:880–889
Ngo P, Ozga JA, Reinecke DM (2002) Specificity of auxin regulation of gibberellin 20-oxidase gene expression in pea pericarp. Plant Mol Biol 49:439–448
Nitsch JP (1970) Hormonal factors in growth and development. In: Hulme AC (ed) The biochemistry of fruits and their products. Academic Press, London, New York, pp 427–472
Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604
Ross JJ, O’Neill DP, Wolbang CM, Symons GM, Reid JB (2002) Auxin-gibberellin interactions and their role in plant growth. J Plant Growth Regul 20:346–353
Seo M, Jikumaru Y, Kamiya Y (2011) Profiling of hormones and related metabolites in seed dormancy and germination studies. Methods Mol Biol 773:99–111
Serrani JC, Sanjuán R, Ruiz-Rivero O, Fos M, García Martínez JL (2007) Gibberellin regulation of fruit set and growth in tomato. Plant Physiol 145:246–257
Serrano M, Martínez-Romero D, Zuzunaga M, Riquelme F, Valero D (2007) Calcium, polyamine and gibberellin treatments to improve postharvest fruit quality. In: Dris R, Jain SM (eds) Production practices and quality assessment of food crops. Vol. 4. Postharvest treatment and technology. Kluwer Academic Publishers, Dordrecht, pp 55–68
Shimada A, Ueguchi-Tanaka M, Nakatsu T, Nakajima M, Naoe Y, Ohmiya H et al (2008) Structural basis for gibberellin recognition by its receptor GID1. Nature 456:520–523
Sponsel VM, Hedden P (2004) Gibberellin biosynthesis and inactivation. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action!. Kluwer Academic Publishers, Dordrecht, pp 63–94
Sun TP (2010) Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant Physiol 154:567–570
Sun TP, Gubler F (2004) Molecular mechanism of gibberellin signalling in plants. Ann Rev Plant Biol 55:197–223
Thomas SG, Philips AL, Hedden P (1999) Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc Natl Acad Sci USA 96:4698–4703
Tyler L, Thomas SG, Hu JH, Dill A, Alonso JM, Ecker JR et al (2004) DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019
Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M et al (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698
Ueguchi-Tanaka M, Nakajim M, Katoh E, Ohmiya H, Asano K, Saji S et al (2007) Molecular interactions of a soluble gibberellin Receptor, GID1, with a rice DELLA protein, SLR1, and Gibberellin. Plant Cell 19:2140–2155
Vargas AM, Le Cunff L, This P, Ibanez J, de Andres MT (2013) VvGAI1 polymorphisms associate with variation for berry traits in grapevine. Euphytica 191:85–91
Wang T, Tomic S, Gabdoulline RR, Wade RC (2004) How optimal are the binding energetics of barnase and barstar? Biophys J 87:1618–1630
Wolbang CM, Chandler PM, Smith JJ, Ross JJ (2004) Auxin from the developing inflorescence is required for the biosynthesis of active gibberellins in barley stems. Plant Physiol 134:769–776
Xu YL, Li L, Gage DA, Zeevaart JAD (1999) Feedback regulation of GA5 expression and metabolic engineering of gibberellin levels in Arabidopsis. Plant Cell 11:927–936
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Ann Rev Plant Biol 59:225–251
Yamaguchi I, Takahashi N (1976) Change of gibberellin and abscisic acid content during fruit development of Prunus persica. Plant Cell Physiol 17:611–614
Yasumura Y, Crumpton-Taylor M, Fuentes S, Harberd NP (2007) Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Curr Biol 17:1225–1230
Acknowledgments
We thank Dr. Stephen G. Thomas for providing gid1a-1/gid1c-1 double mutant, Dr. Stanton Gelvin for providing the EYFP vectors. We also thank the Ontario Ministry of Agriculture, Food and Rural Affairs (OMAFRA) and Early Researchers Award of the Ontario Ministry of Innovation for financial assistance. We thank Dr. Bouzayen for help with subcellular localization experiment.
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PslGID1b (JX569804); gPslGID1b (JX569802); PslGID1c (JX569805); gPslGID1c (JX569803); PslGA3ox1 (JX569806).
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El-Sharkawy, I., Sherif, S., El Kayal, W. et al. Characterization of gibberellin-signalling elements during plum fruit ontogeny defines the essentiality of gibberellin in fruit development. Plant Mol Biol 84, 399–413 (2014). https://doi.org/10.1007/s11103-013-0139-8
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DOI: https://doi.org/10.1007/s11103-013-0139-8