Abstract
In an attempt to functionally characterize a petunia zinc-finger gene ZPT2-10, which is specifically expressed in style transmitting tissue, we fused its cDNA downstream of the potato SK2 promoter (SK2:ZPT2-10) and then introduced it into Petunia hybrida. We found that some transformants had acquired altered traits in compatibility in mating; these were termed ‘transgene-dependent incompatibility (TDI)’. These transgenic lines were fertile when self-pollinated or crossed with other TDI lines. In contrast, they failed to mate when crossed with untransformed wild-type petunia or non-TDI lines of SK2:ZPT2-10 transformants. The TDI phenomenon was observed irrespective of whether the TDI lines were used as the pollen or pistillar parent. The TDI phenotype cosegregated with the SK2:ZPT2-10 transgene in the T1 generation and loss of this transgene resulted in the recovery of normal fertility. In the case of infertile pollination with the TDI line as one parent, pollen tubes grew normally through pistillar tissues, where endogenous ZPT2-10 is expressed, and eventually reached the ovules. However, the resultant embryos were arrested at the globular-heart stage. We found no correlation between the occurrence of the TDI phenotype and the expression of ZPT2-10 transcripts. On the basis of these observations, we discuss the possible molecular mechanisms underlying this phenomena and its utility.
Similar content being viewed by others
References
Adams S, Vinkenoog R, Spielman M, Dickinson HG, Scott RJ (2000) Parent-of-origin effects on seed development in Arabidopsis thaliana require DNA methylation. Development 127:2493–2502
Agarie S, Kai M, Takatsuji H, Ueno O (1997) Expression of C3 and C4 photosynthetic characteristics in the amphibious plant Eleocharis vivipara: structure and analysis of the expression of isogenes for pyruvate, orthophosphate dikinase. Plant Mol Biol 34:363–369
Brink RA, Cooper DC (1947) The endosperm in seed development. Bot Rev 13:423–541
Bushell C, Spielman M, Scott RJ (2003) The basis of natural and artificial postzygotic hybridization barriers in Arabidopsis species. Plant Cell 15:1430–1442
Costa LM, Gutierrez-Marcos JF, Dickinson HG (2004) More than a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci 9:507–514
Dale PJ, Clarke B, Fontes EM (2002) Potential for the environmental impact of transgenic crops. Nat Biotechnol 20:567–574
Daniell H, Datta R, Varma S, Gray S, Lee S-B (1998) Containment of herbicide resistance through genetic engineering of the chloroplast genome. Nat Biotechnol 16:345–348
Ficker M, Wemmer T, Thompson RD (1997) A promoter directing high level expression in pistils of transgenic plants. Plant Mol Biol 35:425–431
Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol 42:819–832
House LR, Nelson OE (1958) Tracer study of pollen-tube growth in cross-sterile maize. J Hered 49:18–21
Johnston SA, den Nijs TPM, Peloquin SJ, Hanneman RE (1980) The significance of genic balance to endosperm development in interspecific cross. Theor Appl Genet 57:5–9
Jorgensen RA, Cluster PD, English J, Que Q, Napoli CA (1996) Chalcone synthase cosuppression phenotypes in petunia flowers: comparison of sense vs. antisense constructs and single-copy vs. complex T-DNA sequences. Plant Mol Biol 31:957–973
Kapoor S, Kobayashi A, Takatsuji H (2002) Silencing of the tapetum-specific zinc finger gene TAZ1 causes premature degeneration of tapetum and pollen abortion in petunia. Plant Cell 14:2353–2367
Kapoor S, Takatsuji H (2006) Silencing of an anther-specific zinc-finger gene, MEZ1, causes aberrant meiosis and pollen abortion in petunia. Plant Mol Biol 61:415–430
Kim JC, Lee SH, Cheong YH, Yoo CM, Lee SI, Chun HJ, Yun DJ, Hong JC, Lee SY, Lim CO, Cho MJ (2001) A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants. Plant J 25:247–259
Kubo K, Kanno Y, Nishino T, Takatsuji H (2000) Zinc-finger genes that specifically express in pistil secretory tissues of petunia. Plant Cell Physiol 41:377–382
Kubo K, Sakamoto A, Kobayashi A, Rybka Z, Kanno Y, Nakagawa H, Takatsuji H (1998) Cys2/His2 zinc-finger protein family of petunia: evolution and general mechanism of target-sequence recognition. Nucleic Acids Res 26:608–615
Kuboyama T, Chung CS, Takeda G (1994) The diversity of interspecific pollen–pistil incongruity in Nicotiana. Sexual Plant Reprod 7:250–258
Mariani C, Beuckeleer Md, Truettner J, Leemans J, Goldberg RB (1990) Induction of male sterility in plants by a chimaeric ribonuclease gene. Nature 347:737–741
Napoli CA, Fahy D, Wang HY, Taylor LP (1999) White anther: a petunia mutant that abolishes pollen flavonol accumulation, induces male sterility, and is complemented by a chalcone synthase transgene. Plant Physiol 120:615–622
Niimi Y (1970) In vitro fertilization in the self-incompatible plant, Petunia hybrida. J Jpn Soc Hort Sci 39:56–62
Niimi Y (1976) Effect of “stylar pollination” on in vitro seed setting of Petunia hybrida. J Jpn Soc Hort Sci 45:168–172
Sijacic P, Wang X, Skirpan AL, Wang Y, Dowd PE, McCubbin AG, Huang S, Kao TH (2004) Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429:302–305
Spielman M, Preuss D, Li FL, Browne WE, Scott RJ, Dickinson HG (1997) TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development 124:2645–2657
Spielman M, Vinkenoog R, Dickinson HG, Scott RJ (2001) The epigenetic basis of gender in flowering plants and mammals. Trends Genet 17:705–711
Sugano S, Kaminaka H, Rybka Z, Catala R, Salinas J, Matsui K, Ohme-Takagi M, Takatsuji H (2003) Stress-responsive zinc finger gene ZPT2-3 plays a role in drought tolerance in petunia. Plant J 36:830–841
Takayama S, Isogai A (2005) Self-incompatibility in plants. Annu Rev Plant Biol 56:467–489
Vinkenoog R, Bushell C, Spielman M, Adams S, Dickinson HG, Scott RJ (2003) Genomic imprinting and endosperm development in flowering plants. Mol Biotechnol 25:149–184
Acknowledgements
We are grateful to Dr. Richard Thompson (Max Planck Institute) for providing the pSK2/1 plasmid. This work was supported in part by a PROBRAIN grant from the Bio-Oriented Technology Research Advancement Institution (BRAIN) of Japan and a Grant-in-Aid for Scientific Research from Japan Society for the Promotion of Science.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kubo, K., Takatsuji, H. Transgene-dependent incompatibility induced by introduction of the SK2:ZPT2-10 chimeric gene in petunia. Transgenic Res 16, 85–97 (2007). https://doi.org/10.1007/s11248-006-9034-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11248-006-9034-2