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Induction of gibberellin 20-oxidases and repression of gibberellin 2β-oxidases in unfertilized ovaries of entire tomato mutant, leads to accumulation of active gibberellins and parthenocarpic fruit formation

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Abstract

In tomato (Solanum lycopersicum L.), auxin and gibberellins (GAs) cross-talk plays an important role during fruit-set. The entire tomato mutant has been previously reported to carry a deletion in the coding region of the SlIAA9 gene, a member of the auxin signal repressor family Aux/IAA. In this paper, we examined the role of ENTIRE gene in controlling GAs metabolism and directing spontaneous fruit initiation and early ovary growth. It was shown that, similarly to pollinated fruits, facultative parthenocarpy in entire depends on active GA metabolism, since fruit growth is suppressed when GA biosynthesis is blocked. Analysis of endogenous GAs during the first 10 days after flower emasculation revealed that entire fruits accumulated higher amounts of active GAs (GA1 and GA3) in comparison to wild type pollinated fruits, suggesting that a different GA homeostasis regulation occurs. Transcript analysis of the main GA biosynthesis genes showed that differently from unpollinated and non parthenocarpic wild type ovaries, in entire active GA flux modulation is regulated by the activation of SlGA20ox1 and SlGA20ox2 and also by a marked reduction of GA catabolism (reduced transcription of GA 2β-oxidase genes) during the early fruit expansion phase.

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Abbreviations

AC:

Ailsa Craig

GA:

Gibberellin

GC–MS/MS:

Gas chromatography-tandem mass spectrometry

Aux/IAA:

Auxin/indoleacetic acid

GA20ox:

GA 20-oxidase

GA3ox:

GA 3β-oxidase

GA2ox:

GA 2β-oxidase

References

  • Aubert D, Chevillard M, Dorne AM, Arlaud G, Herzog M (1998) Expression patterns of GASA genes in Arabidopsis thaliana: the GASA4 gene is up-regulated by gibberellins in meristematic regions. Plant Mol Biol 36:871–883

    Article  CAS  PubMed  Google Scholar 

  • Audran-Delalande C, Bassa C, Mila I, Regad F, Zouine M, Bouzayen M (2012) Genome-wide identification, functional analysis and expression profiling of the Aux/IAA gene family in tomato. Plant Cell Physiol 53:659–672

    Article  CAS  PubMed  Google Scholar 

  • Bangerth F (1989) Dominance among fruits/sinks and the search for a correlative signal. Physiol Plantarum 76:608–614

    Article  CAS  Google Scholar 

  • Ben-Nissan G, Weiss D (1996) The petunia homologue of tomato gast1: transcript accumulation coincides with gibberellin-induced corolla cell elongation. Plant Mol Biol 32:1067–1074

    Article  CAS  PubMed  Google Scholar 

  • Bohner J, Hedden P, Bora-Haber E, Bangerth F (1988) Identification and quantitation of gibberellins in fruits of Lycopersicon esculentum, and their relationship to fruit size in L. esculentum and L. pimpinellifolium. Physiol Plantarum 73:348–353

    Article  CAS  Google Scholar 

  • Bünger-Kibler S, Bangerth F (1982) Relationship between cell number, cell size and fruit size of seeded fruits of tomato (Lycopersicon esculentum Mill.), and those induced parthenocarpically by the application of plant growth regulators. Plant Growth Regul 1:143–154

    Google Scholar 

  • Coles JP, Phillips AL, Crocker SJ, García-Lepe R, Mervyn JL, Hedden P (1999) Modification of gibberellin production and plant development in Arabidopsis by sense and antisense expression of gibberellin 20-oxidase genes. Plant J 17:547–556

    Article  CAS  PubMed  Google Scholar 

  • de Jong M, Wolters-Arts M, García-Martínez JL, Mariani C, Vriezen WH (2011) The Solanum lycopersicum auxin response factor 7 (SlARF7) mediates cross-talk between auxin and gibberellin signalling during tomato fruit set and development. J Exp Bot 62:617–626

    Article  PubMed Central  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  CAS  PubMed  Google Scholar 

  • di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW. InfoStat versión 2012. InfoStat Group, Facultad de Ciencias Agropecuarias, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar

  • Dorcey E, Urbez C, Blázquez MA, Carbonell J, Perez-Amador MA (2009) Fertilization-dependent 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 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451

    Article  PubMed Central  PubMed  Google Scholar 

  • Hagen G, Guilfoyle TJ (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Koenig D, Bayer E, Kang J, Kuhlemeier C, Sinha N (2009) Auxin patterns Solanum lycopersicum leaf morphogenesis. Development 136:2997–3006

    Article  CAS  PubMed  Google Scholar 

  • Koshioka M, Nishijima T, Yamazaki H, Liu Y, Nonaka M, Mander LN (1994) Analysis of gibberellins in growing fruits of Lycopersicon esculentum after pollination or treatment with 4-chlorophenoxyacetic acid. J Hortic Sci 69:171–180

    CAS  Google Scholar 

  • Mapelli S, Frova C, Torti G, Soressi GP (1978) Relationship between set, development and activities of growth regulators in tomato fruits. Plant Cell Physiol 19:1281–1288

    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 Regul 30:405–415

    Article  CAS  Google Scholar 

  • Martí C, Orzáez D, Ellul P, Moreno V, Carbonell J, Granell A (2007) Silencing of DELLA induces facultative parthenocarpy in tomato fruits. Plant J 52:865–876

    Article  PubMed  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 Phisiol 167:1188–1196

    Article  Google Scholar 

  • McGiffen ME, Manthey JA (1996) The role of methanol in promoting plant growth: a current evaluation. Hort Sci 31:1092–1096

    CAS  Google Scholar 

  • Mignolli F, Mariotti L, Lombardi L, Vidoz ML, Ceccarelli N, Picciarelli P (2012) Tomato fruit development in the auxin-resistant dgt mutant is induced by pollination but not by auxin treatment. J Plant Physiol 169:1165–1172

    Article  CAS  PubMed  Google Scholar 

  • Nadeau CD, Ozga JA, Kurepin LV, Jin A, Pharis RP, Reinecke DM (2011) Tissue-specific regulation of gibberellin biosynthesis in developing pea seeds. Plant Physiol 156:897–912

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ngo P, Ozga JA, Reinecke DM (2002) Specificity of auxin regulation of gibberellin 20-oxidase expression in pea pericarp. Plant Mol Biol 49:439–448

    Article  CAS  PubMed  Google Scholar 

  • O’Neill DP, Davidson SE, Clarke VC, Yamauchi Y, Yamaguchi S, Kamiya Y, Reid JB, Ross JJ (2010) Regulation of the gibberellin pathway by auxin and DELLA proteins. Planta 232:1141–1149

    Article  PubMed  Google Scholar 

  • Olimpieri 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  PubMed  Google Scholar 

  • Ozga JA, van Huizen R, Reinecke DM (2002) Hormone and seed-specific regulation of pea fruit growth. Plant Physiol 128:1379–1389

    Article  PubMed Central  CAS  PubMed  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Pattison RJ, Catalá C (2012) Evaluating auxin distribution in tomato (Solanum lycopersicum) through an analysis of the PIN and AUX/LAX gene families. Plant J 70:585–598

    Article  CAS  PubMed  Google Scholar 

  • Rademacher W (2000) Growth retardants: effect on gibberellin biosynthesis and other metabolic pathways. Annu Rev Plant Physiol Plant Mol Biol 51:501–531

    Article  CAS  PubMed  Google Scholar 

  • Rebers M, Kaneta T, Kawaide H, Yamaguchi S, Yang YY, Imai R, Sekimoto H, Kamiya Y (1999) Regulation of gibberellin biosynthesis genes during flower and early fruit development of tomato. Plant J 17:241–250

    Article  CAS  PubMed  Google Scholar 

  • Rowe RN, Farr DJ, Richards BA (1994) Effects of foliar and root application of methanol and ethanol on the growth of tomato plants (Lycopersicum esculentum Mill.). New Zeal J Crop Hort 22:335–337

    Article  CAS  Google Scholar 

  • Ruan YL, Patrick 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 

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

    Article  CAS  Google Scholar 

  • Serrani JC, Sanjuán 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  PubMed Central  CAS  PubMed  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 

  • Shi L, Gast RT, Gopalraj M, Olszewski NE (1992) Characterization of a shoot-specific, GA3- and ABA-regulated gene from tomato. Plant J 2:153–159

    CAS  PubMed  Google Scholar 

  • Sundberg E, Østergaard L (2009) Distinct and dynamic auxin activities during reproductive development. Cold Spring Harb Perspect Biol 1:a001628

    Article  PubMed Central  PubMed  Google Scholar 

  • Thomas SG, Phillips 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vivian-Smith A, Koltunow AM (1999) Genetic analysis of growth-regulator-induced parthenocarpy in Arabidopsis. Plant Physiol 121:437–451

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latché A, Pech JC, Bouzayen M (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17:2676–2692

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang H, Shauer N, Usadel B, Frasse P, Zouine M, Hernould M, Latché A, Pech JC, Fernie AR, Bouzayen M (2009) Regulatory features underlying pollination-dependent and -independent tomato fruit set revealed by transcript and primary metabolite profiling. Plant Cell 21:1428–1452

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Weiss D, Ori N (2007) Mechanism of cross talk between gibberellin and other hormones. Plant Physiol 144:1240–1246

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Worley CK, Zenser N, Ramos J, Rouse D, Leyser O, Theologis A, Callis J (2000) Degradation of Aux/IAA proteins is essential for normal auxin signalling. Plant J 21:553–562

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Peng Z, Liu S, He Y, Cheng L, Kong F, Wang J, Lu G (2012) Genome-wide analysis of Aux/IAA gene family in Solanaceae species using tomato as a model. Mol Genet Genomics 287:295–311

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Cheng R, Xiao J, Quian C, Wang T, Li H, Ouyang B, Ye Z (2007) A single-base deletion mutation in SlIAA9 gene causes tomato (Solanum lycopersicum) entire mutant. J Plant Res 120:671–678

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann R, Sakai H, Hochholdinger F (2010) The Gibberellic acid stimulated-like gene family in maize and its role in lateral root development. Plant Physiol 152:356–365

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Dr. A. Pardossi for providing greenhouse facilities and helpful advice during the plant growing season. We are also grateful to Dr. N. Ceccarelli for his critical remarks about the experimental design.

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Correspondence to Francesco Mignolli.

Electronic supplementary material

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10725_2014_2_MOESM1_ESM.tif

Supplementary material 1 Ratio between GA19 and GA20 plus GA29 concentration in AC pollinated and parthenocarpic entire fruits (TIFF 206 kb)

10725_2014_2_MOESM2_ESM.tif

Supplementary material 2 Diameter of 10-day-old fruits treated with mock (1 % ethanol, 0.1 % Tween 20), 20 ng ovary−1 and 100 ng ovary−1 of the synthetic auxin 4-chlorophenoxyacetic acid (4-CPA) (TIFF 74 kb)

10725_2014_2_MOESM3_ESM.tif

Supplementary material 3 Relationship between flower position in the truss (lower Roman numbers indicate proximity to the stem) and frequency of emasculated flowers that developed parthenocarpic fruits (grey bars) or remained as static ovaries (white bars) (TIFF 124 kb)

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Mignolli, F., Vidoz, M.L., Mariotti, L. et al. Induction of gibberellin 20-oxidases and repression of gibberellin 2β-oxidases in unfertilized ovaries of entire tomato mutant, leads to accumulation of active gibberellins and parthenocarpic fruit formation. Plant Growth Regul 75, 415–425 (2015). https://doi.org/10.1007/s10725-014-0002-1

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  • DOI: https://doi.org/10.1007/s10725-014-0002-1

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