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Biosynthesis and Contents of Gibberellins in Seeded and Seedless Sweet Orange (Citrus sinensis L. Osbeck) Cultivars

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Abstract

In this work, we study the capacity to biosynthesize gibberellins (GA) of ovules (either fertilised or unfertilised), developing seeds and pericarp from fruitlets and their relation with fruit set capacity. Experiments were performed in adult, 12-year-old trees of seeded (Pineapple) and seedless parthenocarpic (Washington navel) sweet orange [Citrus sinensis L. Osbeck] cultivars. The activity of GA20-, GA3- and GA2-oxidases and gibberellin levels were measured in the ovules and pericarp of fruitlets in different development states. The results indicate that ovules are the main sites of gibberellin synthesis in fruitlets during the post-anthesis period. The most intense GA1 synthesis—coincident with the highest expression of GA20ox2, GA3ox1 and GA2ox1—was detected in the ovules of the seeded cultivar, probably induced by fecundation and associated with low early fruitlet abscission rates. By contrast, the low activity detected in the sterile cultivar appears to be rather developmentally or constitutively regulated. As a fruitlet develops, the GA1 concentration is augmented in the pericarp in comparison to ovules or developing seeds, and levels therein did not exhibit noticeable differences between varieties. Furthermore, developing seeds from pineapple had higher GA1 content than the unfertilised abortive ovules from Washington navel. Taken together, data suggest a main role for this hormone in the control of fruitlet abscission, and also demonstrate a function in seed development.

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References

  • Ben-Cheikh W, Perez-Botella J, Tadeo FR, Talón M, Primo-Millo E (1997) Pollination increases gibberellin levels in developing ovaries of seeded varieties of citrus. Plant Physiol 114:557–564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bustin SA (2002) Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J Mol Endocrinol 29:23–39

    Article  CAS  PubMed  Google Scholar 

  • De Jong M, Mariani C, Vriezen WH (2009) The role of auxin and gibberellin in tomato fruit set. J Exp Bot 60:1523–1532

    Article  CAS  PubMed  Google Scholar 

  • Dorcey E, Urbez C, Blázquez MA, Carbonell J, Pérez-Amador MA (2009) Fertilization-depend auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. Plant J 58:318–332

    Article  CAS  PubMed  Google Scholar 

  • Eeuwens CJ, Schwabe WW (1975) Seed and pod wall development in Pisum sativum L. in relation to extracted and applied hormones. J Exp Bot 26:1–14

    Article  CAS  Google Scholar 

  • Erickson L, Brannaman BL (1960) Abscission of reproductive structures and leaves of orange trees. J Am Soc Hort Sci 75:222–229

    Google Scholar 

  • Fos M, Nuez F, García-Martinez JL (2000) The gene pat-2, which induces natural parthenocarpy, alters the gibberellin content in unpollinated tomato ovaries. Plant Physiol 122:471–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fos M, Proano K, Nuez F, García-Martinez JL (2001) Role of gibberellins in parthenocarpic fruit development induced by the genetic system pat-3/pat-4 in tomato. Physiol Plant 111:545–550

    Article  CAS  PubMed  Google Scholar 

  • Frost HB, Soost RK (1968) Seed reproduction: development of gametes and embryos. In: Reuther W, Batchelor LD, Webber HJ (eds) The Citrus Industry, vol 2., University of CaliforniaCalifornia, USA, pp 290–320

    Google Scholar 

  • García-Hurtado N, Carrera E, Ruíz-Rivero O, López-Gresa MP, Hedden P, Gong F, García-Martínez JL (2012) The characterization of transgenic tomato overexpressing gibberellin 20-oxidase reveals induction of parthenocarpic fruit growth, higher yield, and alteration of the gibberellin biosynthetic pathway. J Exp Bot 63:5803–5813

    Article  CAS  PubMed  Google Scholar 

  • García-Martinez JL, García-Papi MA (1979) The influence of gibberellic acid, 2,4-dichlorophenoxyacetic acid and 6-benzylaminopurine on fruit set of Clementine mandarin. Sci Hort 10:285–293

    Article  Google Scholar 

  • García-Martínez JL, Martí M, Sabater T, Maldonado A, Vercher Y (1991a) Development of fertilized ovules and their role in the growth of pea pod. Physiol Plant 83:411–416

    Article  Google Scholar 

  • García-Martínez JL, Santes C, Croker SJ, Hedden P (1991b) Identification, quantitation, and distribution of gibberellins in fruits of Pisum sativum cv. Alaska during pod development. Planta 184:53–60

    Article  PubMed  Google Scholar 

  • García-Martínez JL, López-Díaz M, Sanchez-Beltrán MJ, García-Martínez JL, Phillips AL, Ward DA, Gaskin P, Hedden P (1997) Isolation and transcript analysis of gibberellin 20-oxidase genes in pea and bean in relation to fruit development. Plant Mol Biol 33:1073–1084

    Article  PubMed  Google Scholar 

  • Giacomelli L, Rota-Stabelli O, Masuero D, Acheampong AK, Moretto M, Caputi L (2013) Gibberellin metabolism in Vitis vinifera L. during bloom and fruit set: functional characterization and evolution of grapevine gibberellin oxidases. J Exp Bot 64:4403–4419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez-Cadenas A, Mehouachi J, Tadeo FR, Primo-Millo E, Talón M (2000) Hormonal regulation of fruitlet abscission induced by carbohydrate shortage in citrus. Planta 210:636–643

    Article  PubMed  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acid Res 40:D1178–D1186 (Database issue)

    Article  CAS  PubMed  Google Scholar 

  • Guardiola JL, García-Marí F, Agustí M (1984) Competition and fruit set in the Washington Navel orange. Physiol Plant 62:297–302

    Article  CAS  Google Scholar 

  • Hazra P, Dutta AK, Chatterjee P (2010) Altered gibberellin and auxin levels in the ovaries in the manifestation of genetic parthenocarpy in tomato (Solanum lycopersicum). Curr Sci 99:1439–1443

    CAS  Google Scholar 

  • Hedden P, Thomas SG (2012) Gibberellin biosynthesis and its regulation. Biochem J 444:11–25

    Article  CAS  PubMed  Google Scholar 

  • Huerta L, García-Lor A, García-Martínez JL (2009) Characterization of gibberellin 20-oxidases in the citrus hybrid Carrizo citrange. Tree Physiol 29:569–577

    Article  CAS  PubMed  Google Scholar 

  • Iglesias DJ, Tadeo FR, Primo-Millo E, Talón M (2006) Carbohydrate and ethylene levels related to fruitlet drop through abscission zone A in citrus. Trees 20:348–355

    Article  CAS  Google Scholar 

  • Mariotti L, Picciarelli P, Lombardi L, Ceccarelli N (2011) Fruit set and early fruit growth in tomato are associated with increases in indoleacetic acid, cytokinin, and bioactive gibberellin contents. J Plant Growth Reg 30:405–415

    Article  CAS  Google Scholar 

  • Martí E, Carrera E, Ruiz-Rivero O, García-Martínez JL (2010) Hormonal regulation of tomato gibberellin 20-oxidase1 expressed in Arabidopsis. J Plant Physiol 167:1188–1196

    Article  CAS  PubMed  Google Scholar 

  • Medina M, Roque E, Oineda B, Cañas L, Rodriguez-Concepción M, Beltrán JP, Gómez-Mena C (2013) Early anther ablation triggers parthenocarpic fruit development in tomato. Plant Biotechnol J 11:770–779

    Article  CAS  PubMed  Google Scholar 

  • Mehouachi J, Serna D, Zaragoza S, Agustí M, Talón M, Primo Millo E (1995) Defoliation increases fruit abscission and reduces carbohydrate levels in developing fruits and woody tissues of Citrus unshiu. Plant Sci 107:189–197

    Article  CAS  Google Scholar 

  • Mehouachi J, Iglesias DJ, Tadeo FR, Agustí M, Primo-Millo E, Talón M (2000) The role of leaves in citrus fruitlet abscission: effects on endogenous gibberellins levels and carbohydrate content. J Hort Sci Biotechnol 75:79–85

    CAS  Google Scholar 

  • Mesejo C, Yuste R, Martinez-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 (C. clementina). Physiol Plant 148:187–196

    Article  CAS  Google Scholar 

  • O´Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue 0. Protoplasma 59:368–373

    Article  Google Scholar 

  • Ollimpieri I, Siligato F, Caccia R, Mariotti L, Ceccarelli N, Soressi GP, Mazzucato A (2007) Tomato fruit set driven by pollination or by the parthenocarpic fruit allele are mediated by transcriptionally regulated gibberellin biosynthesis. Planta 226:877–888

    Article  CAS  Google Scholar 

  • Ozga JA, Reinecke DM (2003) Hormonal interactions in fruit development. J Plant Growth Reg 22:73–81

    Article  CAS  Google Scholar 

  • Ozga JA, Reinecke DM, Ayele BT, Ngo P, Nadeau C, Wickramarathna AD (2009) Developmental and hormonal regulation of gibberellin biosynthesis and catabolism in pea fruit. Plant Physiol 150:448–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poling SM (1991) Identification of endogenous gibberellins in immature navel orange fruit. J Agric Food Chem 39:677–680

    Article  CAS  Google Scholar 

  • Rodrigo MJ, García-Martínez JL, Santes CM, Gaskin P, Hedden P (1997) The role of gibberellins A(1) and A(3) in fruit growth of Pisum sativum L and the identification of gibberellins A(4) and A(7) in young seeds. Planta 201:446–455

    Article  CAS  Google Scholar 

  • Ruan YL, Patric JW, Bouzayen M, Osorio S, Fernie AR (2012) Molecular regulation of seed and fruit set. Trends Plant Sci 17:656–665

    Article  CAS  PubMed  Google Scholar 

  • Santes CM, Hedden P, Gaskin P, García-Martínez JL (1995) Gibberellins and related compounds in young fruits of pea and their relationship to fruit set. Phytochemistry 40:1347–1355

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Serfontein CM, Catling HD (1968) Determining the canopy area of citrus trees. S Afr Citrus J 413:14–15

    Google Scholar 

  • Serrani JC, Fos M, Atares A, García-Martínez JL (2007a) Effect of gibberellin and auxin on parthenocarpic fruit growth induction in the cv micro-torn of tomato. J Plant Growth Reg 26:211–221

    Article  CAS  Google Scholar 

  • Serrani JC, Sanjuan R, Ruiz-Rivero O, Fos M, García-Martínez JL (2007b) Gibberellin regulation of fruit set and growth in tomato. Plant Physiol 145:246–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Serrani JC, Ruiz-Rivero O, Fos M, García-Martínez JL (2008) Auxin-induced fruit-set in tomato is mediated in part by gibberellins. Plant J 56:922–934

    Article  CAS  PubMed  Google Scholar 

  • Tadeo FR, Tudela D, Primo-Millo E (1995) 1-Aminocyclopropane-1- carboxylic acid-induced ethylene stimulates callus formation by cell enlargement in the cambial region of internodal explants of citrus. Plant Sci 110:113–119

    Article  CAS  Google Scholar 

  • Talón M, Hedden P, Primo-Millo E (1990a) Gibberellins in Citrus sinensis: a comparison between seeded and seedless varieties. J Plant Growth Reg 9:201–206

    Article  Google Scholar 

  • Talón M, Zacarías L, Primo-Millo E (1990b) Hormonal changes associated with fruit set and development in mandarins differing in their parthenocarpic ability. Physiol Plant 79:400–406

    Article  Google Scholar 

  • Talón M, Zacarías L, Primo-Millo E (1992) Gibberellins and parthenocarpic ability in developing ovaries of seedless mandarins. Plant Physiol 99:1575–1581

    Article  PubMed  PubMed Central  Google Scholar 

  • Turnbull GCN (1989) Identification and quantitative analysis of gibberellins in Citrus. J Plant Growth Reg 8:273–282

    Article  CAS  Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Ann Rev Plant Biol 59:225–251

    Article  CAS  Google Scholar 

  • Yan J, Yuan F, Long G, Qin L, Deng Z (2012) Selection of reference genes for quantitative real-time RT-PCR analysis in citrus. Mol Biol Reports 39:1831–1838

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Drs. Isabel Lopez-Diaz and Esther Carrera for the hormone quantification carried out at the Plant Hormone Quantification Service, IBMCP, Valencia, Spain. Thanks are due to Teresa Sabater from the IBMCP, for their help. This work has been supported by two research projects, RTA2013-00024-CO2-01 from INIA (Ministerio de Economía y Competitividad, Spain) and IVIA-5423 from Consellería de Agricultura (Generalitat Valenciana, Valencia, Spain).

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Correspondence to Almudena Bermejo or Domingo J. Iglesias.

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Bermejo, A., Martínez-Alcántara, B., Martínez-Cuenca, MR. et al. Biosynthesis and Contents of Gibberellins in Seeded and Seedless Sweet Orange (Citrus sinensis L. Osbeck) Cultivars. J Plant Growth Regul 35, 1036–1048 (2016). https://doi.org/10.1007/s00344-016-9602-5

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