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Tomato fruit set driven by pollination or by the parthenocarpic fruit allele are mediated by transcriptionally regulated gibberellin biosynthesis

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Abstract

We investigated the role of gibberellins (GAs) in the phenotype of parthenocarpic fruit (pat), a recessive mutation conferring parthenocarpy in tomato (Solanum lycopersicum L.). Novel phenotypes that parallel those reported in plants repeatedly treated with gibberellic acid or having a GA-constitutive response indicate that the pat mutant probably expresses high levels of GA. The retained sensitivity to the GA-biosynthesis inhibitor paclobutrazol reveals that this condition is dependent on GA biosynthesis. Expression analysis of genes encoding key enzymes involved in GA biosynthesis shows that in normal tomato ovaries, the GA20ox1 transcript is in low copy number before anthesis and only pollination and fertilization increase its transcription levels and, thus, GA biosynthesis. In the unpollinated ovaries of the pat mutant, this mechanism is de-regulated and GA20ox1 is constitutively expressed, indicating that a high GA concentration could play a part in the parthenocarpic phenotype. The levels of endogenous GAs measured in the floral organs of the pat mutant support such a hypothesis. Collectively, the data indicate that transcriptional regulation of GA20ox1 mediates pollination-induced fruit set in tomato and that parthenocarpy in pat results from the mis-regulation of this mechanism. As genes involved in the control of GA synthesis (LeT6, LeT12 and LeCUC2) and response (SPY) are also altered in the pat ovary, it is suggested that the pat mutation affects a regulatory gene located upstream of the control of fruit set exerted by GAs.

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Abbreviations

CUC2:

Cup-shaped cotyledon2

DAP:

Days after pollination

GA:

Gibberellin

GA3 :

Gibberellic acid

GA20ox:

GA 20-oxidase

GA3ox:

GA 3-oxidase

GC-MS/MS:

Chromatography–tandem mass spectrometry

HAE:

Hours after emasculation

HAP:

Hours after pollination

HBP:

Hours before pollination

HP:

Hand-pollinated

IAA:

Indole-3-acetic acid

KNOX :

Knotted-like homeobox genes

OP:

Open-pollinated

PAC:

Paclobutrazol

Pat:

Parthenocarpic fruit

RT:

Reverse transcription

SPY :

Spindly

WT:

Wild type

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Acknowledgments

We thank Dr. Francesca Tilesi (Dipartimento di Biologia Cellulare e dello Sviluppo, Università La Sapienza, Roma, Italy) and Dr. Dario Beraldi (Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, UK) for their contribution to the early stages in this work; Pietro Mosconi (Dipartimento di Agrobiologia e Agrochimica, Università della Tuscia, Viterbo, Italy) for expert technical assistance and Dr. Giovanna Frugis (Istituto di Biologia e Biotecnologia Agraria, Roma, Italy), Dr. Theo Lange (Institut für Pflanzenbiologie, Technischen Universität Braunschweig, Braunschweig, Germany) and two anonymous reviewers for their valuable comments on the manuscript and Jacqueline Scarpa for help with the English form of the manuscript. This work was supported by the funds from the University of Tuscia for Scientific Research, project “Ruolo delle gibberelline nell’allegagione e nello sviluppo del frutto in pomodoro”.

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Authors and Affiliations

  1. Dipartimento di Agrobiologia e Agrochimica, Sezione di Genetica, Università degli Studi della Tuscia, Via S.C. de Lellis snc, 01100, Viterbo, Italy

    Irene Olimpieri, Francesca Siligato, Riccardo Caccia, Gian Piero Soressi & Andrea Mazzucato

  2. Dipartimento di Biologia delle Piante Agrarie, Università degli Studi di Pisa, Via Mariscoglio, 34, 56124, Pisa, Italy

    Lorenzo Mariotti & Nello Ceccarelli

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  1. Irene Olimpieri
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  2. Francesca Siligato
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  3. Riccardo Caccia
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  4. Gian Piero Soressi
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  5. Andrea Mazzucato
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  6. Lorenzo Mariotti
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Correspondence to Andrea Mazzucato.

Electronic supplementary material

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425_2007_533_MOESM1_ESM.ppt

Fig. S1 The principal pathways of gibberellin (GA) metabolism in higher plants, including the non-early-13-hydroxylated pathway (left branch) and the early-13-hydroxylated pathway (right branch). Arrows connect the precursor with the product of each step and circled numbers refers to the enzymes catalysing the reactions as follows: (1) ent-copalyl diphosphate synthase; (2) ent-kaurene synthase; (3) ent-kaurene 19-oxidase; (4) kaurenoic acid oxidase; (5) GA 13-hydroxylase; (6) GA 20-oxidase (GA20ox); (7) GA 3β-hydroxylase (GA3ox); (8) GA 2-oxidase (GA2ox). Those components of the early-13-hydroxylated pathway that have been monitored in this study are highlighted. (Modified from Hedden and Phillips, 2000). GGPP, geranylgeranyl pyrophosphate (DOC 39 kb)

425_2007_533_MOESM2_ESM.ppt

Fig. S2 Expression analysis of genes involved in GA synthesis and response in WT (white bars) and pat mutant (black bars) tomato ovaries at the time of flower opening (stage 3). RNA was isolated and reverse transcribed using oligo(dT) and Moloney murine leukemia virus-reverse transcriptase. The cDNAs generated were subsequently used in a 25 ml PCR reaction in the presence of primers specific for the studied genes or the ACTIN control. The RT-PCR products were separated on 1.5% (w/v) agarose gels stained with ethidium bromide. Expression data are reported as estimates of relative mRNA amount derived from the ratio between the quantitative values of PCR band intensity for the target gene and the actin control measured by the Gel Analyzer procedure of the ImageJ software (http://rsb.info.nih.gov/ij/). Data points are means of three biological replicates ±SE and * indicates significant differences for P£0.05 between the WT and pat mutant ovaries after one-way analysis of variance (DOC 37 kb)

425_2007_533_MOESM3_ESM.doc

Table S1. Sets of RT-PCR primers and PCR conditions used to amplify tomato gene-specific regions of coding sequences involved in GA biosynthesis and response (DOC 33 kb)

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Olimpieri, I., Siligato, F., Caccia, R. et al. Tomato fruit set driven by pollination or by the parthenocarpic fruit allele are mediated by transcriptionally regulated gibberellin biosynthesis . Planta 226, 877–888 (2007). https://doi.org/10.1007/s00425-007-0533-z

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