Uses a Unique Ligand-Binding Mode for Trapping Opines and Acquiring A Competitive Advantage in the Niche Construction on Plant Host

English version České info

An ecological niche is defined, in a given environment, by the availability of nutritive resources, which can be specifically assimilated by certain living organisms to promote their proliferation. The bacterial pathogen Agrobacterium tumefaciens is able to engineer an ecological niche in the infected host via the transformation of the plant genome and diversion of the plant metabolism towards production of the opine nutrients. In this work, we quantified the selective advantage conferred to a member of the phytopathogenic species A. tumefaciens which is able to assimilate the opine nopaline. This opine is a condensate of arginine and α-ketoglurate that is produced both under linear and cyclic forms in the plant tumour environment. We further determined at the molecular and atomistic levels how A. tumefaciens is able to sense the nopaline molecules, and which metabolic pathways are activated in response. Overall, this work deciphered some key molecular events in the niche construction of the pathogen A. tumefaciens that is unique among living organisms and used to develop bioengineering tools.

Vyšlo v časopise: Uses a Unique Ligand-Binding Mode for Trapping Opines and Acquiring A Competitive Advantage in the Niche Construction on Plant Host. PLoS Pathog 10(10): e32767. doi:10.1371/journal.ppat.1004444
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004444

Souhrn

Zdroje

1. GelvinSB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67 : 16–37.

2. PitzschkeA, HirtH (2010) New insights into an old story: Agrobacterium-induced tumour formation in plants by plant transformation. 29 : 1021–1032.

3. SchellJ, Van MontaguM, De BeuckeleerM, De BlockM, DepickerA, et al. (1979) Interactions and DNA transfer between Agrobacterium tumefaciens, the Ti-plasmid and the plant host. Proc R Soc Lond B Biol Sci 204 : 251–266.

4. Tempé J, Petit A (1983) La piste des opines. In: Pühler A, editor. Molecular genetics of the bacteria-plant interaction. Berlin-Heidelberg: Springer-Verlag. pp. 14–32.

5. DessauxY, PetitA, TempéJ (1993) Chemistry and biochemistry of opines, chemical mediators of parasitism. Phytochem 34 : 31–38.

6. Flores-MirelesAL, EberhardA, WinansSC (2012) Agrobacterium tumefaciens can obtain sulphur from an opine that is synthesized by octopine synthase using S-methylmethionine as a substrate. Mol Microbiol 84 : 845–856.

7. PiperKR, Beck von BodmanS, FarrandSK (1993) Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 362 : 448–450.

8. GuyonP, ChiltonMD, PetitA, TempéJ (1980) Agropine in “null-type” crown gall tumours: Evidence for generality of the opine concept. Proc Natl Acad Sci USA 77 : 2693–2697.

9. BellCR, CummingsNE, CanfieldML, MooreLW (1990) Competition of octopine-catabolizing Pseudomonas spp. and octopine-type Agrobacterium tumefaciens for octopine in chemostats. Appl Environ Microbiol 56 : 2840–2846.

10. WilsonM, SavkaMA, HwangI, FarrandSK, LindowSE (1995) Altered Epiphytic Colonization of Mannityl Opine-Producing Transgenic Tobacco Plants by a Mannityl Opine-Catabolizing Strain of Pseudomonas syringae. Appl Environ Microbiol 61 : 2151–2158.

11. GuyonP, PetitA, TempéJ, DessauxY (1993) Transformed plants producing opines specifically promote growth of opine-degrading agrobacteria. Mol Plant-Microbe Interact 6 : 92–98.

12. OgerP, PetitA, DessauxY (1997) Genetically engineered plants producing opines alter their biological environment. Nat Biotechnol 15 : 369–372.

13. SavkaMA, FarrandSK (1997) Modification of rhizobacterial populations by engineering bacterium utilization of a novel plant-produced resource. Nat Biotechnol 15 : 363–368.

14. SchardlCL, KadoCI (1983) A functional map of the nopaline catabolism genes on the Ti plasmid of Agrobacterium tumefaciens C58. Mol Gen Genet 191 : 10–16.

15. KimH, FarrandSK (1997) Characterization of the acc operon from the nopaline-type Ti plasmid pTiC58, which encodes utilization of agrocinopines A and B and susceptibility to agrocin 84. J Bacteriol 179 : 7559–7572.

16. HallLM, SchrimsherJL, TaylorKB (1983) A new opine derived from nopaline. J Biol Chem 258 : 7276–7279.

17. HernalsteensJP, Thia-ToongL, SchellJ, Van MontaguM (1984) An Agrobacterium-transformed cell culture from the monocot Asparagus officinalis. EMBO J 3 : 3039–3041.

18. OhBH, PanditJ, KangCH, NikaidoK, GokcenS, et al. (1993) Three-dimensional structures of the periplasmic lysine/arginine/ornithine-binding protein with and without a ligand. J Biol Chem 268 : 11348–11355.

19. PlanamenteS, MondyS, HommaisF, VigourouxA, MoréraS, et al. (2013) Structural basis for selective GABA binding in bacterial pathogens. Mol Microbiol 86 : 1085–1099.

20. PlanamenteS, VigourouxA, MondyS, NicaiseM, FaureD, et al. (2010) A conserved mechanism of GABA binding and antagonism is revealed by structure-function analysis of the periplasmic binding protein Atu2422 in Agrobacterium tumefaciens. J Biol Chem 24 : 30294–30303.

21. BerntssonRP, SmitsSH, SchmittL, SlotboomDJ, PoolmanB (2010) A structural classification of substrate-binding proteins. FEBS Lett 584 : 2606–2617.

22. KrissinelE, HenrickK (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 60 : 2256–2268.

23. YaoN, TrakhanovS, QuiochoFA (1994) Refined 1.89-A structure of the histidine-binding protein complexed with histidine and its relationship with many other active transport/chemosensory proteins. Biochem 33 : 4769–4779.

24. OhBH, AmesGF, KimSH (1994) Structural basis for multiple ligand specificity of the periplasmic lysine-, arginine-, ornithine-binding protein. J Biol Chem 269 : 26323–26330.

25. ZankerH, von LintigJ, SchröderJ (1992) Opine transport genes in the octopine (occ) and nopaline (noc) catabolic regions in Ti plasmids of Agrobacterium tumefaciens. J Bacteriol 174 : 841–849.

26. KlapwijkPM, OudshoornM, SchilperoortRA (1977) Inducible permease involved in the uptake of octopine, lysopine and octopinic acid by Agrobacterium tumefaciens strains carrying virulence-associated plasmids. Microbiology 102 : 1–11.

27. SansN, SchröderG, SchröderJ (1987) The Noc region of Ti plasmid C58 codes for arginase and ornithine cyclodeaminase. Eur J Biochem 167 : 81–87.

28. FarrandSK, DessauxY (1986) Proline biosynthesis encoded by the noc and occ loci of Agrobacterium Ti plasmids. J Bacteriol 167 : 732–734.

29. ChoK, FuquaC, WinansSC (1997) Transcriptional regulation and locations of Agrobacterium tumefaciens genes required for complete catabolism of octopine. J Bacteriol 179 : 1–8.

30. SchardlCL, KadoCI (1983) Ti plasmid and chromosomal ornithine catabolism genes of Agrobacterium tumefaciens C58. J Bacteriol 155 : 196–202.

31. LangJ, PlanamenteS, MondyS, DessauxY, MoréraS, et al. (2013) Concerted transfer of the virulence Ti plasmid and companion At plasmid in the Agrobacterium tumefaciens-induced plant tumour. Mol Microbiol 90 : 1178–1189.

32. Von LintigJ, KreuschD, SchroderJ (1994) Opine-regulated promoters and LysR-type regulators in the nopaline (noc) and octopine (occ) catabolic regions of Ti plasmids of Agrobacterium tumefaciens. J Bacteriol 176 : 495–503.

33. Beck von BodmanS, HaymanGT, FarrandSK (1992) Opine catabolism and conjugal transfer of the nopaline Ti plasmid pTiC58 are coordinately regulated by a single repressor. Proc Natl Acad Sci USA 89 : 643–647.

34. WoodDW, SetubalJC, KaulR, MonksDE, KitajimaJP, et al. (2001) The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294 : 2317–2323.

35. SlaterSC, GoldmanBS, GoodnerB, SetubalJC, FarrandSK, et al. (2009) Genome sequences of three agrobacterium biovars help elucidate the evolution of multichromosome genomes in bacteria. J Bacteriol 191 : 2501–2511.

36. RobertsWP, TateME, KerrA (1977) Agrocin 84 is a 6-N-phosphoramidate of an adenine nucleotide analogue. Nature 265 : 379–381.

37. KimJG, ParkBK, KimSU, ChoiD, NahmBH, et al. (2006) Bases of biocontrol: sequence predicts synthesis and mode of action of agrocin 84, the Trojan horse antibiotic that controls crown gall. Proc Natl Acad Sci USA 103 : 8846–8851.

38. BouzarH, MooreLW (1987) Isolation of different agrobacterium biovars from a natural oak savanna and tallgrass prairie. Appl Environ Microbiol 53 : 717–721.

39. BouzarH, OuadahD, KrimiZ, JonesJB, TrovatoM, et al. (1993) Correlative association between resident plasmids and the host chromosome in a diverse Agrobacterium soil population. Appl Environ Microbiol 59 : 1310–1317.

40. DeekenR, EngelmannJC, EfetovaM, CzirjakT, MüllerT, et al. (2006) An integrated view of gene expression and solute profiles of Arabidopsis tumours: a genome-wide approach. Plant Cell 18 : 3617–3634.

41. SavkaMA, BlackRC, BinnsAN, FarrandSK (1996) Translocation and exudation of tumour metabolites in crown galled plants. Mol Plant Microbe Interact 9 : 310–313.

42. Tempé J (1983) Chemistry and biochemistry of open-chain imino-acids. In: Weistein B, editor. Chemistry and biochemistry of amino acids, peptides and proteins. New York: Marcel Dekker Inc. pp. 113–203.

43. McCoyAJ, Grosse-KunstleveRW, AdamsPD, WinnMD, StoroniLC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40 : 658–674.

44. BlancE, RoversiP, VonrheinC, FlensburgC, LeaSM, et al. (2004) Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr D Biol Crystallogr 60 : 2210–2221.

45. EmsleyP1, CowtanK (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60 : 2126–2132.

46. HaudecoeurE, TannièresM, CirouA, RaffouxA, DessauxY, et al. (2009) Different regulation and roles of lactonases AiiB and AttM in Agrobacterium tumefaciens C58. Mol Plant Microbe Interact 22 : 529–537.

47. MachoAP, GuidotA, BarberisP, BeuzónCR, GeninS (2010) A competitive index assay identifies several Ralstonia solanacearum type III effector mutant strains with reduced fitness in host plants. Mol Plant Microbe Interact 23 : 1197–1205.