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

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.

[1]  J. Young,et al.  Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes , 2004, Molecular ecology.

[2]  A. Pühler,et al.  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. , 2008, FEMS microbiology ecology.

[3]  B. Glick,et al.  A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria , 1998, Journal of theoretical biology.

[4]  Soichi Wakatsuki,et al.  Crystal Structure of 1-Aminocyclopropane-1-carboxylate Deaminase from Hansenula saturnus * , 2000, The Journal of Biological Chemistry.

[5]  A. Willems.  The taxonomy of rhizobia: an overview , 2006, Plant and Soil.

[6]  N. Toro,et al.  Plasmids in rhizobia : The role of nonsymbiotic plasmids , 1996 .

[7]  J. Li,et al.  Transcriptional regulation of the Enterobacter cloacae UW4 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene (acdS). , 2001, Canadian journal of microbiology.

[8]  X. Nesme,et al.  During infection of its host, the plant pathogen Ralstonia solanacearum naturally develops a state of competence and exchanges genetic material , 1999 .

[9]  B. Glick,et al.  Identification of DNA sequences that regulate the expression of the Enterobacter cloacae UW4 1-aminocyclopropane-1-carboxylic acid deaminase gene. , 2000, Canadian journal of microbiology.

[10]  B. Glick,et al.  Partial purification and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the plant growth promoting rhizobacterium Pseudomonas putida GR12-2 , 1994 .

[11]  B R Glick,et al.  Isolation and characterization of ACC deaminase genes from two different plant growth-promoting rhizobacteria. , 1998, Canadian journal of microbiology.

[12]  F. Guinel,et al.  Ethylene is involved in the nodulation phenotype of Pisum sativum R50 (sym 16), a pleiotropic mutant that nodulates poorly and has pale green leaves. , 2000, Journal of experimental botany.

[13]  A. Hirsch,et al.  Plant hormones and nodulation: what's the connection? , 1994, Plant Molecular Biology.

[14]  B. Glick,et al.  Prevalence of 1-aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. , 2004, Antonie van Leeuwenhoek.

[15]  Jeffrey H. Miller.  Experiments in molecular genetics , 1972 .

[16]  B. Glick,et al.  Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. , 2003, Physiologia plantarum.

[17]  F. Guinel,et al.  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 , 2002 .

[18]  Joko Prayitno,et al.  The Ethylene-Insensitive sickle Mutant of Medicago truncatula Shows Altered Auxin Transport Regulation during Nodulation1[W] , 2006, Plant Physiology.

[19]  A. Pühler,et al.  Sequence Analysis of the 144-Kilobase Accessory Plasmid pSmeSM11a, Isolated from a Dominant Sinorhizobium meliloti Strain Identified during a Long-Term Field Release Experiment , 2006, Applied and Environmental Microbiology.

[20]  T. Yamada,et al.  Properties, sequence, and synthesis in Escherichia coli of 1-aminocyclopropane-1-carboxylate deaminase from Hansenula saturnus. , 1998, Journal of biochemistry.

[21]  D. Hanahan.  Studies on transformation of Escherichia coli with plasmids. , 1983, Journal of molecular biology.

[22]  Trevor C. Charles,et al.  Expression of an Exogenous 1-Aminocyclopropane-1-Carboxylate Deaminase Gene in Sinorhizobium meliloti Increases Its Ability To Nodulate Alfalfa , 2004, Applied and Environmental Microbiology.

[23]  H. Matsui,et al.  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. , 1997, Bioscience, biotechnology and biochemistry.

[24]  B. Glick.  Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. , 2005, FEMS microbiology letters.

[25]  P. Simonet,et al.  Horizontal gene transfer by natural transformation in soil environment , 2006 .

[26]  M. Honma.  Stereospecific Reaction of 1-Aminocyclopropane-1-Carboxylate Deaminase , 1993 .

[27]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[28]  T. Larue,et al.  Exogenous Ethylene Inhibits Nodulation of Pisum sativum L. cv Sparkle. , 1992, Plant physiology.

[29]  D. Swofford.  PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[30]  Roderic D. M. Page,et al.  TreeView: an application to display phylogenetic trees on personal computers , 1996, Comput. Appl. Biosci..

[31]  P. Nannipieri,et al.  Nucleic Acids and Proteins in Soil , 2006 .

[32]  J. Pech,et al.  Cellular and Molecular Aspects of the Plant Hormone Ethylene , 1993, Current Plant Science and Biotechnology in Agriculture.

[33]  H. Matsui,et al.  Synthesis and degradation of 1-aminocyclopropane-1-carboxylic acid by Penicillium citrinum. , 1999, Bioscience, biotechnology, and biochemistry.

[34]  B. McConkey,et al.  Transcriptional regulation of ACC deaminase gene expression in Pseudomonas putida UW4. , 2008, Canadian journal of microbiology.

[35]  J. Caballero-Mellado,et al.  Rhizobium Phylogenies and Bacterial Genetic Diversity , 1996 .

[36]  G. Laguerre,et al.  Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. , 1997, International journal of systematic bacteriology.

[37]  R. Palacios,et al.  The Rhizobium Genome , 1990 .

[38]  高田 峰雄.  1-アミノシクロプロパン-1-カルボン酸処理が,種々の発育段階のカキ果実のエチレン生成に及ぼす影響 , 1989 .

[39]  N. Peters,et al.  Nodule formation is stimulated by the ethylene inhibitor aminoethoxyvinylglycine. , 1989, Plant physiology.

[40]  Bernard R. Glick,et al.  Rhizobium leguminosarum Biovar viciae 1-Aminocyclopropane-1-Carboxylate Deaminase Promotes Nodulation of Pea Plants , 2003, Applied and Environmental Microbiology.

[41]  Y. Nakamura,et al.  Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. , 2000, DNA research : an international journal for rapid publication of reports on genes and genomes.

[42]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[43]  Tokuji Shimomura,et al.  Metabolism of 1-Aminocyclopropane-1-carboxylic Acid , 1978 .

[44]  J. Beringer.  R factor transfer in Rhizobium leguminosarum. , 1974, Journal of general microbiology.

[45]  W. Hiatt,et al.  Isolation, sequence, and expression in Escherichia coli of the Pseudomonas sp. strain ACP gene encoding 1-aminocyclopropane-1-carboxylate deaminase , 1991, Journal of bacteriology.

[46]  C. Prigent-Combaret,et al.  Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. , 2006, FEMS microbiology ecology.

[47]  K. K. Pal,et al.  Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. , 2004, Microbiological research.

[48]  S. Tabata,et al.  Expression Islands Clustered on the Symbiosis Island of the Mesorhizobium loti Genome , 2004, Journal of bacteriology.

[49]  D. Cook,et al.  A Legume Ethylene-Insensitive Mutant Hyperinfected by Its Rhizobial Symbiont , 1997, Science.

[50]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[51]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[52]  C. Ronson,et al.  Host-specific regulation of symbiotic nitrogen fixation in Rhizobium leguminosarum biovar trifolii. , 2007, Microbiology.

[53]  M. Madhaiyan,et al.  Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense , 2006, Planta.

[54]  B. Glick,et al.  Three newly isolated plant growth-promoting bacilli facilitate the seedling growth of canola, Brassica campestris , 2003 .

[55]  O. N. Allen,et al.  The Leguminosae: A Source Book of Characteristics, Uses and Nodulation , 1981 .

[56]  C. Prigent-Combaret,et al.  Physical organization and phylogenetic analysis of acdR as leucine-responsive regulator of the 1-aminocyclopropane-1-carboxylate deaminase gene acdS in phytobeneficial Azospirillum lipoferum 4B and other Proteobacteria. , 2008, FEMS microbiology ecology.

[57]  Duckchul Park,et al.  Diversity of 16S rDNA sequences of Rhizobium spp. implications for species determinations. , 2004, FEMS microbiology letters.

[58]  R. Webby,et al.  Comparative Sequence Analysis of the Symbiosis Island of Mesorhizobium loti Strain R7A , 2002, Journal of bacteriology.

[59]  Bernard R. Glick,et al.  Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.) , 2005 .

[60]  A. Richardson,et al.  Evidence for Horizontal Transfer of 1-Aminocyclopropane-1-Carboxylate Deaminase Genes , 2005, Applied and Environmental Microbiology.

[61]  T. Vogel,et al.  Intergeneric transfer of chromosomal and conjugative plasmid genes between Ralstonia solanacearum and Acinetobacter sp. BD413. , 2003, Molecular plant-microbe interactions : MPMI.

[62]  P. Newell,et al.  A novel procedure for rapid isolation of plant growth promoting pseudomonads , 1995 .

[63]  Bernard R. Glick,et al.  Promotion of plant growth by ACC deaminase-producing soil bacteria , 2007, European Journal of Plant Pathology.

[64]  R. Bally,et al.  Phase Variation and Genomic Architecture Changes in Azospirillum , 2006, Journal of bacteriology.

[65]  Jonathan P. Bollback,et al.  Bayesian Inference of Phylogeny and Its Impact on Evolutionary Biology , 2001, Science.

[66]  G. Barry,et al.  Control of ethylene synthesis by expression of a bacterial enzyme in transgenic tomato plants. , 1991, The Plant cell.

[67]  G. Goodlass,et al.  Effects of ethylene on root extension and nodulation of pea (Pisum sativum L.) and white clover (Trifolium repens L.) , 1979, Plant and Soil.

[68]  K. Dietz,et al.  Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. , 2001, Canadian journal of microbiology.

[69]  K. Minamisawa,et al.  Expression of the 1-Aminocyclopropane-1-Carboxylic Acid Deaminase Gene Requires Symbiotic Nitrogen-Fixing Regulator Gene nifA2 in Mesorhizobium loti MAFF303099 , 2006, Applied and Environmental Microbiology.

[70]  Lisa C. Crossman,et al.  The genome of Rhizobium leguminosarum has recognizable core and accessory components , 2006, Genome Biology.