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1-Aminocyclopropane-1-Carboxylate (ACC) Deaminase Genes in Rhizobia from Southern Saskatchewan

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An Erratum to this article was published on 19 February 2009

Abstract

A collection of 233 rhizobia strains from 30 different sites across Saskatchewan, Canada was assayed for 1-aminocyclopropane-1-carboxylate (ACC) deaminase activity, with 27 of the strains displaying activity. When all 27 strains were characterized based on 16S rRNA gene sequences, it was noted that 26 strains are close to Rhizobium leguminosarum and one strain is close to Rhizobium gallicum. Polymerase chain reaction (PCR) was used to rapidly isolate ACC deaminase structural genes from the above-mentioned 27 strains; 17 of them have 99% identities with the previously characterized ACC deaminase structural gene (acdS) from R. leguminosarum bv. viciae 128C53K, whereas the other ten strains are 84% identical (864~866/1,020 bp) compared to the acdS from strain 128C53K. Southern hybridization showed that each strain has only one ACC deaminase gene. Using inverse PCR, the region upstream of the ACC deaminase structural genes was characterized for all 27 strains, and 17 of these strains were shown to encode a leucine-responsive regulatory protein. The results are discussed in the context of a previously proposed model for the regulation of bacterial ACC deaminase in R. leguminosarum 128C53K.

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References

  1. Allen ON, Allen EK (1981) The Leguminosae—a source book of characteristics, uses and nodulation. Macmillan Publishers Ltd., London

    Google Scholar 

  2. Amarger N, Macheret V, Laguerre G (1997) Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris. Int J Syst Bacteriol 47:996–1006

    PubMed  CAS  Google Scholar 

  3. Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN, Matveyeva VA, Tsyganov VE, Borisov AY, Tikhonovich IA, Kluge C, Preisfeld A, Dietz KJ, Stepanok VV (2001) Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 47:642–652

    Article  PubMed  CAS  Google Scholar 

  4. Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250

    Article  CAS  Google Scholar 

  5. Beringer JE (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84:188–198

    PubMed  CAS  Google Scholar 

  6. Bertolla F, Frostegard A, Brito B, Nesme X, Simonet P (1999) During infection of its host, the plant pathogen Ralstonia solanacearum naturally develops a state of competence and exchanges genetic material. Mol Plant Microbe Interact 12:467–472

    Article  CAS  Google Scholar 

  7. Blaha D, Prigent-Combaret C, Mirza MS, Moenne-Loccoz Y (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56:455–470

    Article  PubMed  CAS  Google Scholar 

  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  9. Cheng Z, Duncker BP, McConkey BJ, Glick BR (2008) Transcriptional regulation of ACC deaminase gene expression in Pseudomonas putida UW4. Can J Microbiol 54:128–136

    Article  PubMed  CAS  Google Scholar 

  10. Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiol Res 159:371–394

    Article  PubMed  CAS  Google Scholar 

  11. Ghosh S, Penterman JN, Little RD, Chavez R, Glick BR (2003) Three newly isolated plant growth-promoting bacilli facilitate the seedling growth of canola seedlings. Plant Physiol Biochem 41:277–281

    Article  CAS  Google Scholar 

  12. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7

    Article  PubMed  CAS  Google Scholar 

  13. Glick BR, Karaturovic DM, Newell PC (1995) A novel procedure for rapid isolation of plant growth promoting pseudomonads. Can J Microbiol 41:533–536

    CAS  Google Scholar 

  14. Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68

    Article  PubMed  CAS  Google Scholar 

  15. Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339

    Article  CAS  Google Scholar 

  16. Goodlass G, Smith KA (1979) Effect of ethylene on root extension and nodulation of pea (Pisum sativum L.) and white clover (Trifolium repens L.). Plant Soil 51:387–395

    Article  CAS  Google Scholar 

  17. Grichko VP, Glick BR (2000) Identification of DNA sequences that regulate the expression of the Enterobacter cloacae UW4 1-aminocyclopropane-1-carboxylate deaminase gene. Can J Microbiol 46:1159–1165

    Article  PubMed  CAS  Google Scholar 

  18. Guinel FC, Sloetjes LL (2000) Ethylene is involved in the nodulation phenotype of Pisum sativum R50 (sym 16). An pleiotropic mutant that nodulated poorly and has pale green leaves. J Exp Bot 51:885–894

    Article  PubMed  CAS  Google Scholar 

  19. Guinel FC, Geil RD (2002) A model for the development of the rhizobial and arbuscular mycorrhizal symbioses in legumes and its use to understand the roles of ethylene in the establishment of these two symbioses. Can J Bot 80:695–720

    Article  CAS  Google Scholar 

  20. Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580

    Article  PubMed  CAS  Google Scholar 

  21. Hirsch AM, Fang Y (1994) Plant hormones and nodulation: what’s the connection? Plant Mol Biol 26:5–9

    Article  PubMed  CAS  Google Scholar 

  22. Honma M (1993) Stereospecific reaction of 1-aminocyclopropane-1-carboxylate deaminase. In: Pech JC, Latche A, Balague C (eds) Cellular and molecular aspects of the plant hormone ethylene. Kluwer Academic, Dordrecht, pp 111–116

    Google Scholar 

  23. Honma M, Shimomura T (1978) Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem 42:1825–1831

    CAS  Google Scholar 

  24. Hontzeas N, Richardson AO, Belimov A, Safronova V, Abu-Omar MM, Glick BR (2005) Evidence for horizontal transfer of 1-aminocyclopropane-1-carboxylate deaminase genes. Appl Environ Microbiol 71:7556–7558

    Article  PubMed  CAS  Google Scholar 

  25. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314

    Article  PubMed  CAS  Google Scholar 

  26. Jacobson CB, Pasternak JJ, Glick BR (1994) Partial purification and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the plant growth promoting rhizobacterium Pseudomonas putida GR12–2. Can J Microbiol 40:1019–1025

    Article  CAS  Google Scholar 

  27. Jia YJ, Kakuta Y, Sugawara M, Igarashi T, Oki N, Kisaki M, Shoji T, Kanetuna Y, Horita T, Matsui H, Honma M (1999) Synthesis and degradation of 1-aminocyclopropane-1-carboxylic acid by Penicillium citrinum. Biosci Biotechnol Biochem 63:542–549

    Article  PubMed  CAS  Google Scholar 

  28. Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S, Watanabe A, Idesawa K, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Mochizuki Y, Nakayama S, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7:331–338

    Article  PubMed  CAS  Google Scholar 

  29. Kay E, Chabrillat G, Vogel TM, Simonet P (2003) Intergeneric transfer of chromosomal and conjugative plasmid genes between Ralstonia solanacearum and Acinetobacter sp. BD413. Mol Plant Microbe Interact 16:74–82

    Article  CAS  Google Scholar 

  30. Klee HJ, Kishore GM (1992) Control of fruit ripening and senescence in plants. International Patent No. WO 92/12249, European Patent Office, World Intellectual Property Organization.

  31. Klee HJ, Hayford MB, Kretzmer KA, Barry GF, Kishore GM (1991) Control of ethylene synthesis by expression of a bacterial enzyme in transgenic tomato plants. Plant Cell 3:1187–1193

    Article  PubMed  CAS  Google Scholar 

  32. Kuhn S, Stiens M, Pühler A, Schlüter A (2008) Prevalence of pSmeSM11a-like plasmids in indigenous Sinorhizobium meliloti strains isolated in the course of a field release experiment with genetically modified S. meliloti strains. FEMS Microbiol Ecol 63:118–131

    Article  PubMed  CAS  Google Scholar 

  33. Lee KH, LaRue TA (1992) Exogenous ethylene inhibits nodulation of Pisum sativum L. cv Sparkle. Plant Physiol 100:1759–1763

    Article  PubMed  CAS  Google Scholar 

  34. Li J, Glick BR (2001) Transcriptional regulation of the Enterobacter cloacae UW4 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene (acdS). Can J Microbiol 47:259–267

    Article  Google Scholar 

  35. Ma W, Sebestianova SB, Sebestian J, Burd GI, Guinel FC, Glick BR (2003a) Prevalence of 1-aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. Antonie Van Leeuwenhoek 83:285–291

    Article  PubMed  CAS  Google Scholar 

  36. Ma W, Guinel FC, Glick BR (2003b) Rhizobium leguminosarum biovar viciae 1-aminocyclopropane-1-carboxylate deaminase promotes nodulation of pea plants. Appl Environ Microbiol 69:4396–4402

    Article  PubMed  CAS  Google Scholar 

  37. Ma W, Charles TC, Glick BR (2004) Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in Sinorhizobium meliloti increases its ability to nodulate alfalfa. Appl Environ Microbiol 70:5891–5897

    Article  PubMed  CAS  Google Scholar 

  38. Madhaiyan M, Poonguzhali S, Ryu JH, Sa TM (2006) Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense. Planta 224:268–278

    Article  PubMed  CAS  Google Scholar 

  39. Martínez-Romero E, Palacios R (1990) The Rhizobium genome. CRC Crit Rev Plant Sci 9:59–93

    Article  Google Scholar 

  40. Martínez-Romero E, Caballero-Mellado J (1996) Rhizobium phylogenies and bacterial genetic diversity. CRC Crit Rev Plant Sci 15:113–140

    Article  Google Scholar 

  41. Mercade-Blanco J, Toro N (1996) Plasmids in rhizobia: the role of nonsymbiotic plasmids. Mol Plant Microbe Interact 9:535–545

    Google Scholar 

  42. Mercier A, Kay E, Simonet P (2006) Horizontal gene transfer by natural transformation in soil environment. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soils. Springer, Berlin, pp 355–373

    Chapter  Google Scholar 

  43. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, p 431

    Google Scholar 

  44. Miller SH, Elliot RM, Sullivan JT, Ronson CW (2007) Host-specific regulation of symbiotic nitrogen fixation in Rhizobium leguminosarum bv. trifolii. NCBI GenBank. Accession number: EF165535

  45. Minami R, Uchiyama K, Murakami T, Kawai J, Mikami K, Yamada T, Yokoi D, Ito H, Matsui H, Honma M (1998) Properties, sequence, and synthesis in Escherichia coli of 1-aminocyclopropane-1-carboxylate deaminase from Hansenula saturnus. J Biochem 123:1112–1118

    PubMed  CAS  Google Scholar 

  46. Murakami T, Kiuchi M, Ito H, Matsui H, Honma M (1997) Substitutions of alanine for cysteine at a reactive thiol site and for lysine at a pyridoxal phosphate binding site of 1-aminocyclopropane-1-carboxylate deaminase. Biosci Biotechnol Biochem 61:506–509

    PubMed  CAS  Google Scholar 

  47. Nukui N, Minamisawa K, Ayabe SI, Aoki T (2006) Expression of the 1-aminocyclopropane-1-carboxylic acid deaminase gene requires symbiotic nitrogen-fixing regulator gene nifA2 in Mesorhizobium loti MAFF303099. Appl Environ Microbiol 72:4964–4969

    Article  PubMed  CAS  Google Scholar 

  48. Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  49. Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275:527–530

    Article  PubMed  CAS  Google Scholar 

  50. Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15

    Article  PubMed  CAS  Google Scholar 

  51. Peters NK, Crist-Estes DK (1989) Nodule formation is stimulated by the ethylene inhibitor aminoethoxyvinylglycine. Plant Physiol 91:690–693

    Article  PubMed  CAS  Google Scholar 

  52. Posada D, Crandall KA (1998) Model test: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  53. Prayitno J, Rolfe BG, Mathesius U (2006) The ethylene-insensitive sickle mutant of Medicago truncatula shows altered auxin transport regulation during nodulation. Plant Physiol 142:168–180

    Article  PubMed  CAS  Google Scholar 

  54. Prigent-Combaret C, Blaha D, Pothier JF, Vial L, Poirier M-A, Wisniewski-Dyé F, Moënne-Loccoz Y (2008) Physical organization and phylogenetic analysis of acdR as leucine-responsive regulator of the 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene acdS in phytobeneficial Azospirillum lipoferum 4B and other Proteobacteria. FEMS Microbiol Ecol DOI 10.1111/j.1574-6941.2008.00474.x

  55. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  56. Sambrook J, Russell RW (2001) Molecular cloning: a laboratory manual 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  57. Shah S, Li J, Moffat BA, Glick BR (1998) Isolation and characterization of ACC deaminase genes from two different plant growth promoting rhizobacteria. Can J Microbiol 44:833–843

    Article  PubMed  CAS  Google Scholar 

  58. Sheehy RE, Honma M, Yamada M, Sasaki T, Martineau B, Hiatt WR (1991) Isolation, sequence, and expression in Escherichia coli of the Pseudomonas sp. strain ACP gene encoding 1-aminocyclopropane-1-carboxylate deaminase. J Bacteriol 173:5260–5265

    PubMed  CAS  Google Scholar 

  59. Stiens M, Schneiker S, Keller M, Kuhn S, Puhler A, Schluter A (2006) Sequence analysis of the 144-kilobase accessory plasmid pSmeSM11a, isolated from a dominant Sinorhizobium meliloti strain identified during a long-term field release experiment. Appl Environ Microbiol 72:3662–3672

    Article  PubMed  CAS  Google Scholar 

  60. Sullivan JT, Trzebiatowski JR, Cruickshank RW, Guozy J, Brown SD, Elliot RM, Fleetwood DJ, McCallum NG, Rossbach U, Stuart GS, Weaver JE, Webby RJ, DeBruijn FJ, Ronson CW (2002) Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J Bacteriol 184:3086–3095

    Article  PubMed  CAS  Google Scholar 

  61. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  62. Uchiumi T, Ohwada T, Itakura M, Mitsui H, Nukui N, Dawadi P, Kaneko T, Tabata S, Yokoyama T, Tejima K, Saeki K, Omori H, Hayashi M, Maekawa T, Sriprang R, Murooka Y, Tajima S, Simomura K, Nomura M, Suzuki A, Shimoda Y, Sioya K, Abe M, Minamisawa K (2004) Expression islands clustered on the symbiosis island of the Mesorhizobium loti genome. J Bacteriol 186:2439–2448

    Article  PubMed  CAS  Google Scholar 

  63. Vial L, Lavire C, Mavingui P, Blaha D, Haurat J, Moënne-Loccoz Y, Bally R, Wisniewski-Dyé F (2006) Phase variation and genomic architecture changes in Azospirillum. J Bacteriol 188:5364–5373

    Article  PubMed  CAS  Google Scholar 

  64. Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287:3–14

    Article  CAS  Google Scholar 

  65. Yao M, Ose T, Suqimoto H, Horiuchi A, Nakagawa A, Wakatsuki S, Yokoi D, Murakami T, Honma M, Tanaka I (2000) Crystal structure of 1-aminocyclopropane-1-carboxylate deaminase from Hansenula saturnus. J Biol Chem 275:34557–34565

    Article  PubMed  CAS  Google Scholar 

  66. Young JPW, Mutch LA (2004) Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes. Mol Ecol 13:2435–2444

    Article  PubMed  CAS  Google Scholar 

  67. Young JPW, Mutch LA, Ashford DA, Zézé A, Mutch KE (2003) The molecular evolution of host specificity in the rhizobium–legume symbiosis. In: Hails R, Godfray HCJ, Beringer J (eds) Genes in the Environment. Blackwell Science, Oxford, pp 245–257

    Google Scholar 

  68. Young JM, Park DC, Weir BS (2004) Diversity of 16S rDNA sequences of Rhizobium spp. implications for species determinations. FEMS Microbiol Lett 238:125–131

    PubMed  CAS  Google Scholar 

  69. Young JP, Crossman LC, Johnston AW, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson AR, Todd JD, Poole PS, Mauchline TH, East AK, Quail MA, Churcher C, Arrowsmith C, Cherevach I, Chillingworth T, Clarke K, Cronin A, Davis P, Fraser A, Hance Z, Hauser H, Jagels K, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Sanders M, Simmonds M, Whitehead S, Parkhill J (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7:R34

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was funded by grants from the Natural Sciences and Engineering Research Council of Canada to B. R. Glick. We thank Philom Bios Inc. (Saskatoon, Saskatchewan, Canada) for providing the bacterial strains used in this study.

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  1. Department of Biology, University of Waterloo, 200 University Avenue West, Waterloo, ON, N2L 3G1, Canada

    Jin Duan, Kirsten M. Müller, Trevor C. Charles, Susanne Vesely & Bernard R. Glick

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  1. Jin Duan
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  2. Kirsten M. Müller
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  3. Trevor C. Charles
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Correspondence to Jin Duan.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s00248-009-9493-0

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Duan, J., Müller, K.M., Charles, T.C. et al. 1-Aminocyclopropane-1-Carboxylate (ACC) Deaminase Genes in Rhizobia from Southern Saskatchewan. Microb Ecol 57, 423–436 (2009). https://doi.org/10.1007/s00248-008-9407-6

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