Regulation of Oncogene Expression in T-DNA-Transformed Host Plant Cells

English version České info

Crown gall development requires the expression of agrobacterial genes in the plant host. These genes are transferred by the T-DNA of the plant pathogen Agrobacterium tumefaciens and include the oncogenes IaaH, IaaM and Ipt, which, according to the tumor-inducing principle, are essential for crown gall development. The oncogenes are involved in auxin and cytokinin production. This results, when at appropriate hormone ratios, in enhanced cell proliferation. The T-DNA transformation process and the encoded oncogene enzymes have been intensively studied, but knowledge of oncogene expression in plant cells and the regulatory host factors is missing. We set out to fill this gap, providing evidence that expression of the Ipt gene is host-cell controlled, whereas the IaaH and IaaM genes are ubiquitously expressed at low levels in T-DNA transformed tissue. This is achieved by A. tumefaciens, which first hijacks transcription factors of the plant pathogen response pathway to activate Ipt oncogene expression and initiates cell proliferation. With increasing auxin levels during the infection process, a transcription factor of the auxin-signaling pathway is recruited, potentiating Ipt gene expression. Thus, for crown gall development, two host-signaling pathways are combined through the interaction of transcription factors that adjust the ratio of cytokinin to auxin.

Vyšlo v časopise: Regulation of Oncogene Expression in T-DNA-Transformed Host Plant Cells. PLoS Pathog 11(1): e32767. doi:10.1371/journal.ppat.1004620
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004620

Souhrn

Zdroje

1. Chilton MD, Drummond MH, Merio DJ, Sciaky D, Montoya AL, et al. (1977) Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis. Cell 11: 263–271. 890735

2. Zhu J, Oger PM, Schrammeijer B, Hooykaas PJ, Farrand SK, et al. (2000) The bases of crown gall tumorigenesis. J Bacteriol 182: 3885–3895. 10869063

3. Garfinkel DJ, Simpson RB, Ream LW, White FF, Gordon MP, et al. (1981) Genetic analysis of crown gall: fine structure map of the T-DNA by site-directed mutagenesis. Cell 27: 143–153. 6276020

4. Joos H, Inze D, Caplan A, Sormann M, Van Montagu M, et al. (1983) Genetic analysis of T-DNA transcripts in nopaline crown galls. Cell 32: 1057–1067. 6839358

5. Britton M, Escobar M, Dandekar A (2008) The Oncogenes of Agrobacterium Tumefaciens and Agrobacterium Rhizogenes. In: Tzfira T, Citovsky V, editors. Agrobacterium: From Biology to Biotechnology: Springer New York. pp. 523–563.

6. Garfinkel DJ, Nester EW (1980) Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism. J Bacteriol 144: 732–743. 6253441

7. Schroder G, Waffenschmidt S, Weiler EW, Schroder J (1984) The T-region of Ti plasmids codes for an enzyme synthesizing indole-3-acetic acid. Eur J Biochem 138: 387–391. 6365544

8. Thomashow LS, Reeves S, Thomashow MF (1984) Crown gall oncogenesis: evidence that a T-DNA gene from the Agrobacterium Ti plasmid pTiA6 encodes an enzyme that catalyzes synthesis of indoleacetic acid. Proc Natl Acad Sci U S A 81: 5071–5075. 6089175

9. Thomashow MF, Hugly S, Buchholz WG, Thomashow LS (1986) Molecular basis for the auxin-independent phenotype of crown gall tumor tissues. Science 231: 616–618. 3511528

10. Escobar MA, Dandekar AM (2003) Agrobacterium tumefaciens as an agent of disease. Trends Plant Sci 8: 380–386.

11. Gray J, Wang J, Gelvin SB (1992) Mutation of the miaA gene of Agrobacterium tumefaciens results in reduced vir gene expression. J Bacteriol 174: 1086–1098. 1735704

12. Gray J, Gelvin SB, Meilan R, Morris RO (1996) Transfer RNA Is the Source of Extracellular Isopentenyladenine in a Ti-Plasmidless Strain of Agrobacterium tumefaciens. Plant Physiol 110: 431–438. 12226194

13. Akiyoshi DE, Regier DA, Gordon MP (1987) Cytokinin production by Agrobacterium and Pseudomonas spp. J Bacteriol 169: 4242–4248. 3624204

14. Hwang HH, Wang MH, Lee YL, Tsai YL, Li YH, et al. (2010) Agrobacterium-produced and exogenous cytokinin-modulated Agrobacterium-mediated plant transformation. Mol Plant Pathol 11: 677–690. doi: 10.1111/j.1364-3703.2010.00637.x 20696005

15. Hwang HH, Yang FJ, Cheng TF, Chen YC, Lee YL, et al. (2013) The Tzs protein and exogenous cytokinin affect virulence gene expression and bacterial growth of Agrobacterium tumefaciens. Phytopathology 103: 888–899. doi: 10.1094/PHYTO-01-13-0020-R 23593941

16. Morris RO (1986) Genes Specifying Auxin and Cytokinin Biosynthesis in Phytopathogens. Annual Review of Plant Physiology 37: 509–538.

17. Chateau S, Sangwan RS, Sangwan-Norreel BS (2000) Competence of Arabidopsis thaliana genotypes and mutants for Agrobacterium tumefaciens-mediated gene transfer: role of phytohormones. J Exp Bot 51: 1961–1968. 11141170

18. Sardesai N, Lee LY, Chen H, Yi H, Olbricht GR, et al. (2013) Cytokinins secreted by agrobacterium promote transformation by repressing a plant myb transcription factor. Sci Signal 6: ra100. doi: 10.1126/scisignal.2004518 24255177

19. Veselov D, Langhans M, Hartung W, Aloni R, Feussner I, et al. (2003) Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid. Planta 216: 512–522. 12520344

20. Lee CW, Efetova M, Engelmann JC, Kramell R, Wasternack C, et al. (2009) Agrobacterium tumefaciens promotes tumor induction by modulating pathogen defense in Arabidopsis thaliana. Plant Cell 21: 2948–2962. doi: 10.1105/tpc.108.064576 19794116

21. Cooper GM (2000) The Cell: A Molecular Approach. 2nd edition.

22. Goldberg SB, Flick JS, Rogers SG (1984) Nucleotide sequence of the tmr locus of Agrobacterium tumefaciens pTi T37 T-DNA. Nucleic Acids Res 12: 4665–4677. 6330678

23. Klee H, Montoya A, Horodyski F, Lichtenstein C, Garfinkel D, et al. (1984) Nucleotide sequence of the tms genes of the pTiA6NC octopine Ti plasmid: two gene products involved in plant tumorigenesis. Proc Natl Acad Sci U S A 81: 1728–1732. 6584906

24. Nester EW, Gordon MP, Amasino RM, Yanofsky MF (1984) Crown Gall—a Molecular And Physiological Analysis. Annual Review Of Plant Physiology And Plant Molecular Biology 35: 387–413.

25. de Pater BS, de Kam RJ, Hoge JH, Schilperoort RA (1987) Effects of mutations in the TATA box region of the Agrobacterium T-cyt gene on its transcription in plant tissues. Nucleic Acids Res 15: 8283–8292. 3671084

26. Neuteboom ST, Hulleman E, Schilperoort RA, Hoge JH (1993) In planta analysis of the Agrobacterium tumefaciens T-cyt gene promoter: identification of an upstream region essential for promoter activity in leaf, stem and root cells of transgenic tobacco. Plant Mol Biol 22: 923–929. 8358039

27. Neuteboom ST, Stoffels A, Hulleman E, Memelink J, Schilperoort RA, et al. (1993) Interaction between the tobacco DNA-binding activity CBF and the cyt-1 promoter element of the Agrobacterium tumefaciens T-DNA gene T-CYT correlates with cyt-1 directed gene expression in multiple tobacco tissue types. Plant J 4: 525–534. 8220494

28. Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10: 366–371. 17644023

29. Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51: 21–37. 12602888

30. Ullrich CI, Aloni R (2000) Vascularization is a general requirement for growth of plant and animal tumours. Journal Of Experimental Botany 51: 1951–1960. 11141169

31. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10: 453–460.

32. Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276: 1865–1868. 9188533 9188533

33. Hayashi K (2012) The interaction and integration of auxin signaling components. Plant Cell Physiol 53: 965–975. 22433459 22433459

34. Peer WA (2013) From perception to attenuation: auxin signalling and responses. Curr Opin Plant Biol 16: 561–568. doi: 10.1016/j.pbi.2013.08.003 24004572 doi: 10.1016/j.pbi.2013.08.003 24004572

35. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963–1971.

36. Tiwari SB, Wang XJ, Hagen G, Guilfoyle TJ (2001) AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13: 2809–2822.

37. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435: 441–445. 15917797 15917797

38. Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435: 446–451. 15917798 15917798

39. Calderon Villalobos LI, Lee S, De Oliveira C, Ivetac A, Brandt W, et al. (2012) A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nat Chem Biol 8: 477–485. doi: 10.1038/nchembio.926 22466420 doi: 10.1038/nchembio.926 22466420

40. Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414: 271–276. 11713520 11713520

41. Yamamoto YY, Ichida H, Abe T, Suzuki Y, Sugano S, et al. (2007) Differentiation of core promoter architecture between plants and mammals revealed by LDSS analysis. Nucleic Acids Res 35: 6219–6226. 17855401 17855401

42. Yamamoto YY, Ichida H, Matsui M, Obokata J, Sakurai T, et al. (2007) Identification of plant promoter constituents by analysis of local distribution of short sequences. BMC Genomics 8: 67. 17346352 17346352

43. Prestridge DS (1991) SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements. Comput Appl Biosci 7: 203–206. 2059845 2059845

44. Higo K, Ugawa Y, Iwamoto M, Higo H (1998) PLACE: a database of plant cis-acting regulatory DNA elements. Nucleic Acids Res 26: 358–359. 9847208 9847208

45. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27: 297–300. 9847208 9847208

46. Deeken R, Engelmann JC, Efetova M, Czirjak T, Muller T, et al. (2006) An integrated view of gene expression and solute profiles of Arabidopsis tumors: a genome-wide approach. Plant Cell 18: 3617–3634. 17172353 17172353

47. Jin J, Zhang H, Kong L, Gao G, Luo J (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42: D1182–1187. doi: 10.1093/nar/gkt1016 24174544 doi: 10.1093/nar/gkt1016 24174544

48. Wehner N, Hartmann L, Ehlert A, Bottner S, Onate-Sanchez L, et al. (2011) High-throughput protoplast transactivation (PTA) system for the analysis of Arabidopsis transcription factor function. Plant J 68: 560–569. doi: 10.1111/j.1365-313X.2011.04704.x 21749507 doi: 10.1111/j.1365-313X.2011.04704.x 21749507

49. Xu X, Chen C, Fan B, Chen Z (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18: 1310–1326. 16603654 16603654

50. Pandey SP, Roccaro M, Schon M, Logemann E, Somssich IE (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. Plant J 64: 912–923. doi: 10.1111/j.1365-313X.2010.04387.x 21143673 doi: 10.1111/j.1365-313X.2010.04387.x 21143673

51. Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17: 1405–1411. 9482737 9482737

52. Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, et al. (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17: 444–463. 15659631 15659631

53. Ulmasov T, Hagen G, Guilfoyle TJ (1999) Dimerization and DNA binding of auxin response factors. Plant J 19: 309–319. 10476078 10476078

54. Lau S, De Smet I, Kolb M, Meinhardt H, Jurgens G (2011) Auxin triggers a genetic switch. Nat Cell Biol 13: 611–615. doi: 10.1038/ncb2212 21478855 doi: 10.1038/ncb2212 21478855

55. Krogan NT, Ckurshumova W, Marcos D, Caragea AE, Berleth T (2012) Deletion of MP/ARF5 domains III and IV reveals a requirement for Aux/IAA regulation in Arabidopsis leaf vascular patterning. New Phytol 194: 391–401. doi: 10.1111/j.1469-8137.2012.04064.x 22320407 doi: 10.1111/j.1469-8137.2012.04064.x 22320407

56. Citovsky V, Kozlovsky SV, Lacroix B, Zaltsman A, Dafny-Yelin M, et al. (2007) Biological systems of the host cell involved in Agrobacterium infection. Cell Microbiol 9: 9–20. 17222189 17222189

57. Pitzschke A, Hirt H (2010) New insights into an old story: Agrobacterium-induced tumour formation in plants by plant transformation. EMBO J 29: 1021–1032. doi: 10.1038/emboj.2010.8 20150897 doi: 10.1038/emboj.2010.8 20150897

58. Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, et al. (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315: 1098–1103. 17185563 17185563

59. Chen H, Lai Z, Shi J, Xiao Y, Chen Z, et al. (2010) Roles of arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10: 281. doi: 10.1186/1471-2229-10-281 21167067 doi: 10.1186/1471-2229-10-281 21167067

60. Liu ZQ, Yan L, Wu Z, Mei C, Lu K, et al. (2012) Cooperation of three WRKY-domain transcription factors WRKY18, WRKY40, and WRKY60 in repressing two ABA-responsive genes ABI4 and ABI5 in Arabidopsis. J Exp Bot 63: 6371–6392. doi: 10.1093/jxb/ers293 23095997 doi: 10.1093/jxb/ers293 23095997

61. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5: 199–206. 10785665 10785665

62. Ulker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7: 491–498. 15337090 15337090

63. Wu KL, Guo ZJ, Wang HH, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12: 9–26. 16106749 16106749

64. Sakai H, Honma T, Aoyama T, Sato S, Kato T, et al. (2001) ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294: 1519–1521. 11691951 11691951

65. Taniguchi M, Sasaki N, Tsuge T, Aoyama T, Oka A (2007) ARR1 directly activates cytokinin response genes that encode proteins with diverse regulatory functions. Plant Cell Physiol 48: 263–277. 17202182 17202182

66. Wenzel CL, Schuetz M, Yu Q, Mattsson J (2007) Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana. Plant J 49: 387–398. 17217464 17217464

67. Chi Y, Yang Y, Zhou Y, Zhou J, Fan B, et al. (2013) Protein-protein interactions in the regulation of WRKY transcription factors. Mol Plant 6: 287–300. 23455420 23455420

68. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462–469. 14555774 14555774

69. Nour-Eldin HH, Hansen BG, Norholm MH, Jensen JK, Halkier BA (2006) Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res 34: e122. 17000637 17000637

70. Tzfira T, Tian GW, Lacroix B, Vyas S, Li J, et al. (2005) pSAT vectors: a modular series of plasmids for autofluorescent protein tagging and expression of multiple genes in plants. Plant Mol Biol 57: 503–516. 15821977 15821977

71. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565–1572. 17585298 17585298

72. Heidekamp F, Dirkse WG, Hille J, van Ormondt H (1983) Nucleotide sequence of the Agrobacterium tumefaciens octopine Ti plasmid-encoded tmr gene. Nucleic Acids Res 11: 6211–6223. 6312414 6312414

73. de Pater BS, Klinkhamer MP, Amesz PA, de Kam RJ, Memelink J, et al. (1987) Plant expression signals of the Agrobacterium T-cyt gene. Nucleic Acids Res 15: 8267–8281. 3671083 3671083

74. Lichtenstein C, Klee H, Montoya A, Garfinkel D, Fuller S, et al. (1984) Nucleotide sequence and transcript mapping of the tmr gene of the pTiA6NC octopine Ti-plasmid: a bacterial gene involved in plant tumorigenesis. J Mol Appl Genet 2: 354–362. 6330262 6330262