Translation Start Sequences Affect the Efficiency of Silencing of Agrobacterium Tumefaciens T-DNA Oncogenes

Overview

Journal Plant Physiol

Specialty Physiology

Date 2003 Sep 16

PMID 12972655

Citations 10

Authors

Hyewon Lee

Jodi L Humann

Jennifer S Pitrak

Josh T Cuperus

T Dawn Parks

Cheryl A Whistler

Machteld C Mok

L Walt Ream

Affiliations

Soon will be listed here.

Abstract

Agrobacterium tumefaciens oncogenes cause transformed plant cells to overproduce auxin and cytokinin. Two oncogenes encode enzymes that convert tryptophan to indole-3-acetic acid (auxin): iaaM (tryptophan mono-oxygenase) and iaaH (indole-3-acetamide hydrolase). A third oncogene (ipt) encodes AMP isopentenyl transferase, which produces cytokinin (isopentenyl-AMP). Inactivation of ipt and iaaM (or iaaH) abolishes tumorigenesis. Because adequate means do not exist to control crown gall, we created resistant plants by introducing transgenes designed to elicit posttranscriptional gene silencing (PTGS) of iaaM and ipt. Transgenes that elicit silencing trigger sequence-specific destruction of the inducing RNA and messenger RNAs with related sequences. Although PTGS has proven effective against a variety of target genes, we found that a much higher percentage of transgenic lines silenced iaaM than ipt, suggesting that transgene sequences influenced the effectiveness of PTGS. Sequences required for oncogene silencing included a translation start site. A transgene encoding a translatable sense-strand RNA from the 5' end of iaaM silenced the iaaM oncogene, but deletion of the translation start site abolished the ability of the transgene to silence iaaM. Silencing A. tumefaciens T-DNA oncogenes is a new and effective method to produce plants resistant to crown gall disease.

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References

Moore L . Use of Agrobacterium radiobacter in agricultural ecosystems. Microbiol Sci. 1988; 5(3):92-5. View

Jorgensen R, Atkinson R, Forster R, Lucas W . An RNA-based information superhighway in plants. Science. 1998; 279(5356):1486-7. DOI: 10.1126/science.279.5356.1486. View

Cogoni C, Macino G . Posttranscriptional gene silencing in Neurospora by a RecQ DNA helicase. Science. 1999; 286(5448):2342-4. DOI: 10.1126/science.286.5448.2342. View

Que Q, Wang H, English J, Jorgensen R . The Frequency and Degree of Cosuppression by Sense Chalcone Synthase Transgenes Are Dependent on Transgene Promoter Strength and Are Reduced by Premature Nonsense Codons in the Transgene Coding Sequence. Plant Cell. 1997; 9(8):1357-1368. PMC: 157003. DOI: 10.1105/tpc.9.8.1357. View

Nam J, Matthysse A, Gelvin S . Differences in susceptibility of Arabidopsis ecotypes to crown gall disease may result from a deficiency in T-DNA integration. Plant Cell. 1997; 9(3):317-33. PMC: 156921. DOI: 10.1105/tpc.9.3.317. View

Baulcombe D . DNA events. An RNA microcosm. Science. 2002; 297(5589):2002-3. DOI: 10.1126/science.1077906. View

Fire A, Xu S, Montgomery M, Kostas S, Driver S, Mello C . Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998; 391(6669):806-11. DOI: 10.1038/35888. View

Dougherty W, Parks T . Transgenes and gene suppression: telling us something new?. Curr Opin Cell Biol. 1995; 7(3):399-405. DOI: 10.1016/0955-0674(95)80096-4. View

Llave C, Xie Z, Kasschau K, Carrington J . Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science. 2002; 297(5589):2053-6. DOI: 10.1126/science.1076311. View

10.

Tijsterman M, Ketting R, Plasterk R . The genetics of RNA silencing. Annu Rev Genet. 2002; 36:489-519. DOI: 10.1146/annurev.genet.36.043002.091619. View

11.

Tuschl T, Zamore P, Lehmann R, Bartel D, Sharp P . Targeted mRNA degradation by double-stranded RNA in vitro. Genes Dev. 2000; 13(24):3191-7. PMC: 317199. DOI: 10.1101/gad.13.24.3191. View

12.

Akiyoshi D, Klee H, Amasino R, Nester E, Gordon M . T-DNA of Agrobacterium tumefaciens encodes an enzyme of cytokinin biosynthesis. Proc Natl Acad Sci U S A. 1984; 81(19):5994-8. PMC: 391845. DOI: 10.1073/pnas.81.19.5994. View

13.

Buchmann I, Marner F, Schroder G, Waffenschmidt S, Schroder J . Tumour genes in plants: T-DNA encoded cytokinin biosynthesis. EMBO J. 1985; 4(4):853-9. PMC: 554271. DOI: 10.1002/j.1460-2075.1985.tb03710.x. View

14.

Montgomery M, Xu S, Fire A . RNA as a target of double-stranded RNA-mediated genetic interference in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1998; 95(26):15502-7. PMC: 28072. DOI: 10.1073/pnas.95.26.15502. View

15.

Zamore P, Tuschl T, Sharp P, Bartel D . RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell. 2000; 101(1):25-33. DOI: 10.1016/S0092-8674(00)80620-0. View

16.

Napoli C, Lemieux C, Jorgensen R . Introduction of a Chimeric Chalcone Synthase Gene into Petunia Results in Reversible Co-Suppression of Homologous Genes in trans. Plant Cell. 1990; 2(4):279-289. PMC: 159885. DOI: 10.1105/tpc.2.4.279. View

17.

Smith H, Swaney S, Parks T, Wernsman E, Dougherty W . Transgenic plant virus resistance mediated by untranslatable sense RNAs: expression, regulation, and fate of nonessential RNAs. Plant Cell. 1994; 6(10):1441-53. PMC: 160532. DOI: 10.1105/tpc.6.10.1441. View

18.

Kennerdell J, Carthew R . Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell. 1999; 95(7):1017-26. DOI: 10.1016/s0092-8674(00)81725-0. View

19.

van der Krol A, Mur L, Beld M, Mol J, Stuitje A . Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell. 1990; 2(4):291-9. PMC: 159886. DOI: 10.1105/tpc.2.4.291. View

20.

Tanzer M, Thompson W, LAW M, Wernsman E, Uknes S . Characterization of Post-Transcriptionally Suppressed Transgene Expression That Confers Resistance to Tobacco Etch Virus Infection in Tobacco. Plant Cell. 1997; 9(8):1411-1423. PMC: 157007. DOI: 10.1105/tpc.9.8.1411. View