Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1999 Apr;151(4):1581–1589. doi: 10.1093/genetics/151.4.1581

A new Ac-like transposon of Arabidopsis is associated with a deletion of the RPS5 disease resistance gene.

A D Henk 1, R F Warren 1, R W Innes 1
PMCID: PMC1460570  PMID: 10101179

Abstract

The RPS5 and RFL1 disease resistance genes of Arabidopsis ecotype Col-0 are oriented in tandem and are separated by 1.4 kb. The Ler-0 ecotype contains RFL1, but lacks RPS5. Sequence analysis of the RPS5 deletion region in Ler-0 revealed the presence of an Ac-like transposable element, which we have designated Tag2. Southern hybridization analysis of six Arabidopsis ecotypes revealed 4-11 Tag2-homologous sequences in each, indicating that this element is ubiquitous in Arabidopsis and has been active in recent evolutionary time. The Tag2 insertion adjacent to RFL1 was unique to the Ler-0 ecotype, however, and was not present in two other ecotypes that lack RPS5. DNA sequence from the latter ecotypes lacked a transposon footprint, suggesting that insertion of Tag2 occurred after the initial deletion of RPS5. The deletion breakpoint contained a 192-bp insertion that displayed hallmarks of a nonhomologous DNA end-joining event. We conclude that loss of RPS5 was caused by a double-strand break and subsequent repair, and cannot be attributed to unequal crossing over between resistance gene homologs.

Full Text

The Full Text of this article is available as a PDF (238.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Botella M. A., Coleman M. J., Hughes D. E., Nishimura M. T., Jones J. D., Somerville S. C. Map positions of 47 Arabidopsis sequences with sequence similarity to disease resistance genes. Plant J. 1997 Nov;12(5):1197–1211. doi: 10.1046/j.1365-313x.1997.12051197.x. [DOI] [PubMed] [Google Scholar]
  3. Doseff A., Martienssen R., Sundaresan V. Somatic excision of the Mu1 transposable element of maize. Nucleic Acids Res. 1991 Feb 11;19(3):579–584. doi: 10.1093/nar/19.3.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ellis J., Lawrence G., Ayliffe M., Anderson P., Collins N., Finnegan J., Frost D., Luck J., Pryor T. Advances in the molecular genetic analysis of the flax-flax rust interaction. Annu Rev Phytopathol. 1997;35:271–291. doi: 10.1146/annurev.phyto.35.1.271. [DOI] [PubMed] [Google Scholar]
  5. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  6. Gorbunova V., Levy A. A. Non-homologous DNA end joining in plant cells is associated with deletions and filler DNA insertions. Nucleic Acids Res. 1997 Nov 15;25(22):4650–4657. doi: 10.1093/nar/25.22.4650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Grant M. R., McDowell J. M., Sharpe A. G., de Torres Zabala M., Lydiate D. J., Dangl J. L. Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15843–15848. doi: 10.1073/pnas.95.26.15843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hammond-Kosack Kim E., Jones Jonathan D. G. PLANT DISEASE RESISTANCE GENES. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):575–607. doi: 10.1146/annurev.arplant.48.1.575. [DOI] [PubMed] [Google Scholar]
  9. Hebsgaard S. M., Korning P. G., Tolstrup N., Engelbrecht J., Rouzé P., Brunak S. Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information. Nucleic Acids Res. 1996 Sep 1;24(17):3439–3452. doi: 10.1093/nar/24.17.3439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hulbert S. H. Structure and evolution of the rp1 complex conferring rust resistance in maize. Annu Rev Phytopathol. 1997;35:293–310. doi: 10.1146/annurev.phyto.35.1.293. [DOI] [PubMed] [Google Scholar]
  11. Innes R. W., Bisgrove S. R., Smith N. M., Bent A. F., Staskawicz B. J., Liu Y. C. Identification of a disease resistance locus in Arabidopsis that is functionally homologous to the RPG1 locus of soybean. Plant J. 1993 Nov;4(5):813–820. doi: 10.1046/j.1365-313x.1993.04050813.x. [DOI] [PubMed] [Google Scholar]
  12. Jia Y., Loh Y. T., Zhou J., Martin G. B. Alleles of Pto and Fen occur in bacterial speck-susceptible and fenthion-insensitive tomato cultivars and encode active protein kinases. Plant Cell. 1997 Jan;9(1):61–73. doi: 10.1105/tpc.9.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jones D. A., Thomas C. M., Hammond-Kosack K. E., Balint-Kurti P. J., Jones J. D. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science. 1994 Nov 4;266(5186):789–793. doi: 10.1126/science.7973631. [DOI] [PubMed] [Google Scholar]
  14. Liu D., Crawford N. M. Characterization of the putative transposase mRNA of Tag1, which is ubiquitously expressed in Arabidopsis and can be induced by Agrobacterium-mediated transformation with dTag1 DNA. Genetics. 1998 Jun;149(2):693–701. doi: 10.1093/genetics/149.2.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Luck J. E., Lawrence G. J., Finnegan E. J., Jones D. A., Ellis J. G. A flax transposon identified in two spontaneous mutant alleles of the L6 rust resistance gene. Plant J. 1998 Nov;16(3):365–369. doi: 10.1046/j.1365-313x.1998.00306.x. [DOI] [PubMed] [Google Scholar]
  16. Martin G. B., Brommonschenkel S. H., Chunwongse J., Frary A., Ganal M. W., Spivey R., Wu T., Earle E. D., Tanksley S. D. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science. 1993 Nov 26;262(5138):1432–1436. doi: 10.1126/science.7902614. [DOI] [PubMed] [Google Scholar]
  17. McDowell J. M., Dhandaydham M., Long T. A., Aarts M. G., Goff S., Holub E. B., Dangl J. L. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell. 1998 Nov;10(11):1861–1874. doi: 10.1105/tpc.10.11.1861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Moreno M. A., Chen J., Greenblatt I., Dellaporta S. L. Reconstitutional mutagenesis of the maize P gene by short-range Ac transpositions. Genetics. 1992 Aug;131(4):939–956. doi: 10.1093/genetics/131.4.939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Parker J. E., Coleman M. J., Szabò V., Frost L. N., Schmidt R., van der Biezen E. A., Moores T., Dean C., Daniels M. J., Jones J. D. The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell. 1997 Jun;9(6):879–894. doi: 10.1105/tpc.9.6.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Parniske M., Hammond-Kosack K. E., Golstein C., Thomas C. M., Jones D. A., Harrison K., Wulff B. B., Jones J. D. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell. 1997 Dec 12;91(6):821–832. doi: 10.1016/s0092-8674(00)80470-5. [DOI] [PubMed] [Google Scholar]
  21. Quigley F., Dao P., Cottet A., Mache R. Sequence analysis of an 81 kb contig from Arabidopsis thaliana chromosome III. Nucleic Acids Res. 1996 Nov 1;24(21):4313–4318. doi: 10.1093/nar/24.21.4313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Richter T. E., Pryor T. J., Bennetzen J. L., Hulbert S. H. New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics. 1995 Sep;141(1):373–381. doi: 10.1093/genetics/141.1.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rinehart T. A., Dean C., Weil C. F. Comparative analysis of non-random DNA repair following Ac transposon excision in maize and Arabidopsis. Plant J. 1997 Dec;12(6):1419–1427. doi: 10.1046/j.1365-313x.1997.12061419.x. [DOI] [PubMed] [Google Scholar]
  24. Simonich M. T., Innes R. W. A disease resistance gene in Arabidopsis with specificity for the avrPph3 gene of Pseudomonas syringae pv. phaseolicola. Mol Plant Microbe Interact. 1995 Jul-Aug;8(4):637–640. doi: 10.1094/mpmi-8-0637. [DOI] [PubMed] [Google Scholar]
  25. Song W. Y., Pi L. Y., Wang G. L., Gardner J., Holsten T., Ronald P. C. Evolution of the rice Xa21 disease resistance gene family. Plant Cell. 1997 Aug;9(8):1279–1287. doi: 10.1105/tpc.9.8.1279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Thomas C. M., Jones D. A., Parniske M., Harrison K., Balint-Kurti P. J., Hatzixanthis K., Jones J. D. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell. 1997 Dec;9(12):2209–2224. doi: 10.1105/tpc.9.12.2209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tsay Y. F., Frank M. J., Page T., Dean C., Crawford N. M. Identification of a mobile endogenous transposon in Arabidopsis thaliana. Science. 1993 Apr 16;260(5106):342–344. doi: 10.1126/science.8385803. [DOI] [PubMed] [Google Scholar]
  28. Warren R. F., Henk A., Mowery P., Holub E., Innes R. W. A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell. 1998 Sep;10(9):1439–1452. doi: 10.1105/tpc.10.9.1439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wessler S., Tarpley A., Purugganan M., Spell M., Okagaki R. Filler DNA is associated with spontaneous deletions in maize. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8731–8735. doi: 10.1073/pnas.87.22.8731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Whitham S., Dinesh-Kumar S. P., Choi D., Hehl R., Corr C., Baker B. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell. 1994 Sep 23;78(6):1101–1115. doi: 10.1016/0092-8674(94)90283-6. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES