Abstract
The endogenous levels of 13 gibberellins (GAs), three cytokinins (CKs), abscisic acid (ABA), indole-3-acetic acid (IAA) and jasmonic acid (JA) were analyzed in naturally pollinated ovaries of three mandarin cultivars selected for their different capacity to produce seeds and their differing parthenocarpic ability. The varieties compared were Murcott (pollen self-compatible, highly seeded), Moncada (self-incompatible, moderately seeded), and Moncalina (pollen sterile, seedless), obtained from Moncada by bud γ-irradiation. As expected, the 13-hydroxylation pathway was predominant in ovaries and our results further indicate that cultivar differences exist in GA metabolism. The active gibberellin GA1 levels in ovaries seems to be related with presence of fertilized ovules and, therefore, with the ability to produce the seeds of a variety. Sterility gamma irradiation arrested the biosynthesis of GA1 and its precursor GA19 in Moncalina ovaries if compared to Moncada. The productive efficiency of the studied cultivars also indicated that fruit set depends strongly on the GA1 level achieved by ovaries, which is also closely related with carbohydrate content. The study of the expression of gibberellin-oxidase genes showed that the pollination/fecundation process enhances GA20ox2 and GA3ox1 activities in naturally pollinated Murcott and Moncada ovaries compared with unpollinated Murcott and Moncalina, respectively. GA2ox1 expression was lower in the ovaries of the highly seeded cultivar Murcott than in those of Moncada or Moncalina. Unpollinated Murcott ovaries contained much lower levels of GA1 and IAA than the naturally pollinated ovaries of this cultivar. Conversely, unpollinated ovaries, which exhibited 100 % abscission, had more ABA and JA contents. Cytokinin activity seemed constitutive and independent of pollination/fecundation. However, trans-zeatin (t-Z) and 2-isopentenyl adenine (2-IP) concentrations were higher in Murcott ovaries than in Moncada/Moncalina.

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References
Ali-Dinar HM, Krezdorn AH, Wheaton TA (1988) The sexual-hormonal relation in citrus during fruit set. Acta Hortic 218:159–175
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
Bermejo A, Pardo J, Cano A (2011) Influence of gamma irradiation on seedless citrus production: pollen germination and fruit quality. Food Nutr Sci 2:169–180
Brewbaker JL, Kwack BH (1963) The essential role of calcium ion in pollen germination and pollen tube growth. Am J Bot 50:859–865
Bustin SA (2002) Quantification of mRNA using real-time reversetranscription PCR (RT-PCR): trends and problems. J Mol Endocrinol 29:23–39
Castle WS, Phillips RL (1980) Performance of ‘Marsh’ grapefruit and ‘Valencia’ orange trees on eighteen rootstocks in close planting. J Am Soc Hortic Sci 105:496–499
De Jong M, Mariani C, Vriezen WH (2009) The role of auxin and gibberellin in tomato fruit set. J Exp Bot 60:1523–1532
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 California, California, pp 290–320
Gambetta G, Gravina A, Fasiolo C, Fornero C, Galiger S, Inzaurralde C, Rey F (2013) Self-incompatibility, parthenocarpy and reduction of seed presence in “Afourer” mandarin. Sci Hortic 164:183–188
García-Martínez JL, García-Papi MA (1979) The influence of gibberellic acid, 2,4-dichlorophenoxyacetic acid and 6-benzylaminopurine on fruit set of Clementine mandarin. Sci Hortic 10:285–293
García-Papi MA, García-Martínez JL (1984) Endogenous plant growth substances content in young fruits of seeded and seedless Clementine mandarin as related to fruit set and development. Sci Hortic 22:265–274
Giacomelli L, Rota-Stabelli O, Masuero D, Acheampong AK, Moretto M, Caputi L, Vrhovsek U, Moser C (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
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acid Research, 40 (Database issue): D1178–D1186
Goren R, Huberman M, Goldschmidt E (2003) Girdling: physiological and horticultural aspects. Hortic Rev 30:1–36
Hearn CJ (1986) Development of seedless grapefruit cultivars through budwood irradiation. J Am Soc Hort Sci 111:304–306
Hernandez-Miñana FM, Primo-Millo E (1989) Endogenous cytokinins in developing fruits of seeded and seedless Citrus cultivars. J Exp Bot 40:1127–1134
Hernandez-Miñana FM, Primo-Millo E (1990) Studies on endogenous cytokinins in Citrus. J Hort Sci 65:596–601
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
Iglesias DJ, Tadeo FR, Primo-Millo E, Talón M (2003) Fruit set dependence on carbohydrate availability in citrus trees. Tree Physiol 23:199–204
Ledbetter CA, Ramming DW (1989) Seedlessness in grapes. Hortic Rev 11:159–184
Mariotti L, Picciarelli P, Lombardi L, Ceccarelli N (2011) Fruit set and early fruit growth in tomato are associated with increases in indolacetic acid, cytokinin and bioactive gibberellin contents. J Plant Growth Reg. 30:405–415
Martí E, Carrera E, Ruiz-Rivero García-Martínez JL (2010) Hormonal regulation of tomato gibberellin 20-oxidase1 expressed in Arabidopsis. J Plant Physiol 167:1188–1196
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
Mesejo C, Martínez-Fuentes A, Reig C, Rivas F, Agustí M (2006) The inhibitory effect of CuSO4 on citrus pollen germination and pollen tube growth and its application for the production of seedless fruit. Plant Sci 170:37–43
Mesejo C, Martínez-Fuentes A, Reig C, Agustí M (2008) Gibberellic acid impairs fertilization in Clementine mandarin under cross-pollination conditions. Plant Sci 175:267–271
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 (C. clementina). Physiol Plant 148:87–96
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
Ortiz JM, Zaragoza S, Bono R (1988) The major citrus cultivars in Spain. HortScience 23:691–693
Ozga JA, Reinecke DM (2003) Hormonal interactions in fruit development. J Plant Growth Regul 22:73–81
Ozga JA, Reinecke DM, Ayele BT (2009) Developmental and hormonal regulation of gibberellin biosynthesis and catabolism in pea fruit. Plant Physiol 150:448–462
Powell AA, Krezdorn AH (1977) Influence of fruit-setting treatments on translocation of 14C-metabolites in citrus during flowering and fruiting. J Am Soc Hortic Sci 102:709–714
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
Ruan YL, Patric JW, Bouzayen M, Osorio S, Fernie AR (2012) Molecular regulation of seed and fruit set. Trends Plant Sci 17:656–665
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
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 (2007a) Gibberellin regulation of fruit set and growth in tomato. Plant Physiol 145:246–257
Serrani JC, Fos M, Atares A, García-Martínez JL (2007b) Effect of gibberellin and auxin on parthenocarpic fruit growth induction in the cv micro-torn of tomato. J Plant Growth Reg 26:211–221
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
Soost RK, Cameron JW (1980) “Oroblanco” a triploid pummel x grapefruit hybrid. HortScience 15:667–669
Spiegel-Roy P, Goldschmidt EE (1996) Biology of Citrus. Cambridge University Press, Cambridge, p 244
Talón M, Hedden P, Primo-Millo E (1990a) Gibberellins in Citrus sinensis: a comparison between seeded and seedless varieties. J Plant Growth Regul 9:201–206
Talón M, Zacarías L, Primo-Millo E (1990b) Hormonal changes associated with fruit set and development in mandarins differing in their parthenoarpic ability. Physiol Plant 79:400–406
Talón M, Zacarías L, Primo-Millo E (1992) Gibberellins and parthenocarpic ability in developing ovaries of seedless mandarins. Plant Physiol 99:1575–1581
Vardi A, Levin I, Carmi N (2008) Induction of seedlessness in citrus: from classical techniques to emerging biotechnological approaches. J Am Soc Hort Sci 133:117–126
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Ann Rev Plant Biol 59:225–251
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 Rep 39:1831–1838
Ye W, Qin Z, Ye J, Teixeira da Silva A, Zhang L, Wu X, Lin S, Hu G (2009) Seedless mechanism of a new mandarin cultivar “Wuzishatangju” (Citrus reticulata Blanco). Plant Sci 177:19–27
Zacarías L, Talón M, Ben-Cheikh W, Lafuente MT, Primo-Millo E (1995) Abscisic acid increases in non-growing and paclobutrazol-treated fruits of seedless mandarins. Physiol Plant 95:613–619
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. This work has been supported by two research Projects, RTA2011-00052-00-00 and RTA2011-00114-00-00, from INIA (Ministerio de Educación y Ciencia, Spain), by the European Community FEDER and ESF funds, and by the Consellería de Agricultura, Pesca y Alimentación (Generalitat Valenciana, Spain).
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Bermejo, A., Primo-Millo, E., Agustí, M. et al. Hormonal Profile in Ovaries of Mandarin Varieties with Differing Reproductive Behaviour. J Plant Growth Regul 34, 584–594 (2015). https://doi.org/10.1007/s00344-015-9492-y
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DOI: https://doi.org/10.1007/s00344-015-9492-y


