Abstract
The molecular signals for the development of the ovary into fruit following ovule fertilization are not clear. However, in many species, including tomato (Lycopersicon esculentum Mill.), auxins and auxin transport inhibitors can substitute for fertilization as activators of fruit set, suggesting that this plant hormone plays a key role in this process. In agreement, transgenes for auxin biosynthesis expressed under ovary- or ovule-specific promoters were shown earlier to enable parthenocarpic (i.e. seedless) fruit development. In the present study, we tested an alternative approach for the induction of parthenocarpy that is based on ovary-specific expression of the Agrobacterium rhizogenes-derived gene rolB. This gene was chosen because rolB transgenic plants manifest several syndromes characteristic of auxin treatment. Tomato plants transformed with a chimeric construct containing the rolB gene fused to the ovary- and young-fruit-specific promoter TPRP-F1 developed parthenocarpic fruits. Fruit size and morphology, including jelly fill in the locules of the seedless fruits, were comparable to those of seeded fruits of the parental line. Although it is not known whether ROLB signals for the same cassette of genes involved in fertilization-dependent fruit development, it clearly activates a battery of genes that enable successful completion of seedless fruit development in tomato.
Similar content being viewed by others
Abbreviations
- IAA:
-
indole-1-acetic acid
- TSS:
-
total soluble solids
- WT:
-
wild type
References
Abad M, Monteiro AA (1989) The use of auxins for the production of greenhouse tomatoes in mild-winter conditions: a review. Sci Hort 38:167–192
An G (1986) Development of plant promoter expression vectors and their use for analysis of differential activity of nopaline synthase promoter in transformed tobacco cells. Plant Physiol 81:86–91
An G, Costal MA, Tepfer D, Gupta HS (1994) Induction of male sterility by pollen-specific expression of rolB gene. Abstractsof the 4th international congress on plant molecular biology, Amsterdam, 1994. Abstr. No. 1850
Bangerth F (1989) Dominance among fruit/sinks and the search for correlative signal. Physiol Plant 76:608–614
Barg R, Salts Y (2000) Method for the induction of genetic parthenocarpy in plants. US Patent 6,114,602
Barg R, Pilowsky M, Shabtai S, Carmi N, Szechtman AD, DedicovaB, Salts Y (1997) The TYLCV-tolerant tomato line MP-1 is characterized by superior transformation competence. J Exp Bot 48:1919–1923
Bercetche J, Chriqui D, Adam S, David C (1987) Morphogenetic and cellular reorientations induced by Agrobacterium rhizogenes (strains 1855, 2659 and 8196) on carrot, pea and tobacco. Plant Sci 52:195–210
Cardarelli M, Marioti D, Pomponi M, Spano L, Capone I, Costantino P (1987) Agrobacterium rhizogenes T-DNA genes capable of inducing hairy root phenotype. Mol Gen Genet 209:475–480
Carmi N (1996) Study of the control of a tomato young fruit specific gene and harnessing its promoter to the rolB gene in attempt to induce parthenocarpy (Hebrew, English abstract). Ph.D. thesis, Hebrew University of Jerusalem
Carmi N, Salts Y, Dedicova B, Shabtai S, Pilowsky M, Barg R (1997) Transgenic parthenocarpy due to specific over-sensitization of the ovary to auxin. Acta Hort 447:579–581
Casas Diaz AV, Hewitt JD, Lapushner D (1987) Effect of parthenocarpy on fruit quality in tomato. J Am Soc Hort Sci 112:634–637
Chilton MD, Tepfer DA, Petit A, David C, Casse-Delbart F, Tempe J (1982) Agrobacterium rhizogenes inserts T-DNA into the genome of host plant root cells. Nature 295:432–434
Dale EC, Ow DW (1991) Gene transfer with subsequent removal of the selection gene from the host genome. Proc Natl Acad Sci USA 88:10558–10562
Delbarre A, Muller P, Imhoff V, Barbier-Brygoo H, Maurel C, Leblanc N, Perrot-Rechenmann, C, Guern J (1994) The rolB gene of Agrobacterium rhizogenes does not increase the auxin sensitivity of tobacco protoplasts by modifying the intracellular auxin concentration. Plant Physiol 105:563–569
Donzella G, Spena A, Rotino GL (2000) Transgenic parthenocarpic eggplants: superior germplasm for increased winter production. Mol Breed 6:79–86
Falavigna A, Badino M, Soressi GP (1978) Potential of monomendelian factors pat in the tomato breeding for industry. Genet Agrar 32:159–160
Ficcadenti N, Sestili S, Pandolfini T, Cirillo C, Rotino GL, Spena A (1999) Genetic engineering of parthenocarpic fruit development in tomato. Mol Breed 5:463–470
Filippini F, Rossi V, Marin O, Trovato M, Costantino P, Downey PM, Lo Schiavo F, Terzi M (1996) A plant oncogene as a phosphatase. Nature 379:499–500
George WL, Scott JM, Splittstoesser WE (1984) Parthenocarpy in tomato. Hort Rev 6:65–84
Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451
Hood EE, Gelvin SB, Melchers LS, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2:208–218
Imanshi S, Hiura I (1975) Relationship between fruit weight and seed content in the tomato. J Jpn Soc Hort Sci 44:33–40
Inze D, Follin A, Van Lijsebettens M, Simoens C, Genetello C, Van Montagu M, Schell J (1984) Genetic analysis of the individual T-DNA genes of Agrobacterium tumefaciens: further evidence that two genes are involved in indole-3-acetic acid synthesis. Mol Gen Genet 194:265–274
Klee H, Horsch R, Hinchee MA, Hein MB, Hoffman NL (1987) The effects of overproduction of two Agrobacterium tumefaciens T-DNA auxin biosynthetic gene products in transgenic petunia plants. Genes Dev 1:86–89
Liu Y, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31:777–786
Lukyanenko AN (1991) Parthenocarpy in tomato. In: Kalloo G (ed) Genetic improvement of tomato. Monographs on theoretical and applied genetics. Springer, Berlin Heidelberg New York, pp 167–177
McCormick S (1991) Transformation of tomato with Agrobacterium tumefaciens. In: Lindsey K (ed) Plant tissue culture manual. Kluwer, Dordrecht, pp B6:1–9
Nilsson O, Olsson O (1997) Getting to the root: the role of the Agrobacterium rhizogenes rol genes in the formation of hairy roots. Physiol Plant 100:463–473
Nilsson O, Croizer A, Schmulling T, Sandberg O, Olsson O (1993) Indole-3-acetic acid homeostasis in transgenic tobacco plants expressing the Agrobacterium rhizogenes rolB gene. Plant J 3:681–689
Pandolfini T, Rotino GL, Camerini S, Defez R, Spena A (2002) Optimisation of transgene action at the post-transcriptional level: high quality parthenocarpic fruits in industrial tomatoes. BMC Biotechnol 2:1
Philouze J, Maisonneuve B (1978a) Heredity of the natural ability to set parthenocarpic fruits in the Soviet variety, Severianin. Tomato Genet Coop 28:12–13
Philouze J, Maisonneuve B (1978b) Heredity of the natural ability to set parthenocarpic fruits in a German line. Tomato Genet Coop 28:12
Picken AJF (1984) A review of pollination and fruit set in the tomato (Lycopersicon esculentum Mill.) J Hort Sci 59:1–13
Rotino GL, Perri E, Zottini M, Sommer H, Spena A (1997) Genetic engineering of parthenocarpic plants. Nat Biotechnol 15:1398–1401
Salts Y, Wachs R, Gruissem W, Barg R (1991) Sequence coding for a novel proline-rich protein preferentially expressed in young tomato fruit. Plant Mol Biol 17:149–150
Salts Y, Kenigsbuch D, Wachs R, Gruissem W, Barg R (1992) DNA sequence of the tomato fruit expressed proline-rich protein gene TPRP-F1 reveals an intron within the 3′-untranslated transcript. Plant Mol Biol 18:407–409
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
Schmulling T, Schell J, Spena A (1988) Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 7:2621–2629
Schmulling T, Fladung M, Grossman K, Schell J (1993) Hormonal control and sensitivity of transgenic tobacco and potato plants expressing single rol genes of Agrobacterium rhizogenes T-DNA. Plant J 3:371–382
Slightom JL, Durand-Tardif M, Jouanin L, Tepfer D (1986) Nucleotide sequence analysis of TL-DNA of Agrobacterium rhizogenes Agropine type plasmid. Identification of open reading frames. J Biol Chem 261:108–121
Stevens MA, Rudich J (1978) Genetic potential for overcoming physiological limitation on adaptability, yield and quality in the tomato. HortScience 13:673–678
Szechtman AD, Salts Y, Carmi N, Shabtai S, Pilowsky M, Barg R (1997) Seedless fruit setting in response to NAM treatment of transgenic tomato expressing the iaaH gene specifically in the ovary. Acta Hort 447:597–698
van Altvorst AC, Bino RJ, van Dijk AJ, Lamers AMJ, Lindhout WH, van der Mark F, Dons JJM (1992) Effects of the introduction of Agrobacterium rhizogenes rol genes on tomato plant and flower development. Plant Sci 83:77–85
Acknowledgements
This research was supported by the USA–Israel BARD foundation, and by the Chief Scientist of the Israeli MOAG Fund. It is contribution No. 137-2002, from the Agricultural Research Organization, The Volcani Center, Bet-Dagan. The plasmid pUC19-B26 (rolB) was kindly provided by Prof. J. Schell, Max Planck Institute, Koln, Germany, and plasmid TR-3 (28S rRNA) was kindly provided by Prof. E. Lifschitz, The Technion, Haifa, Israel. The assistance of Dr. A. Gnizi, The Volcani Center, A.R.O., with the statistical analysis is deeply appreciated.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Carmi, N., Salts, Y., Dedicova, B. et al. Induction of parthenocarpy in tomato via specific expression of the rolB gene in the ovary. Planta 217, 726–735 (2003). https://doi.org/10.1007/s00425-003-1052-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-003-1052-1