Effects of indole-3-acetic acid on Sinorhizobium meliloti survival and on symbiotic nitrogen fixation and stem dry weight production

Applied Microbiology and Biotechnology

Volumn 83, Issue 4, 2009, Pages 727-738

  Imperlini, Esther ^a,b   Bianco, Carmelina ^a   Lonardo, Enza ^a   Camerini, Serena ^a,c   Cermola, Michele ^a   Moschetti, Giancarlo ^d   Defez, Roberto ^a  

^a INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^b IRCCS SDN   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d UNIVERSITY OF PALERMO   (Italy)

Author keywords

Cell survival; Nitrogen fixation; PHB; Starch; Stem dry weight; TCA

Indexed keywords

ACETYL-COA; CELL SURVIVAL; CITRATE SYNTHASE; CONTROL STRAIN; DRY WEIGHT; HYDROXYBUTYRATE; IN-CONTROL; INDOLE-3-ACETIC ACID; KETOGLUTARATE; KEY ENZYMES; MEDICAGO TRUNCATULA; PHB; REDUCTION ACTIVITY; SINORHIZOBIUM MELILOTI; STEM DRY WEIGHT; SYMBIOTIC NITROGEN FIXATION; TCA; TRICARBOXYLIC ACID CYCLE; WILD-TYPE CELLS; WILD-TYPE STRAIN;

ACETIC ACID; ACETYLENE; ACIDS; AMINO ACIDS; BIOCHEMICAL ENGINEERING; BIOCHEMISTRY; BIOSYNTHESIS; CATALYSTS; CELL MEMBRANES; ENZYMES; LIGHTING; NITROGEN; PH EFFECTS; STARCH; STRAIN;

NITROGEN FIXATION;

ACETYL COENZYME A; CITRATE SYNTHASE; INDOLEACETIC ACID; OXOGLUTARATE DEHYDROGENASE; POLY(3 HYDROXYBUTYRIC ACID); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ACETYLENE; BACTERIUM; BIOASSAY; DRY MATTER; ENZYME ACTIVITY; EXPERIMENTAL STUDY; HORMONE; LEGUME; METABOLISM; NITROGEN FIXATION; NODULATION; REDUCTION; STARCH; STEM; SURVIVAL; SYMBIOSIS;

ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; BACTERIAL SURVIVAL; CARBOHYDRATE METABOLISM; CELL VIABILITY; CITRIC ACID CYCLE; CONTROLLED STUDY; ENZYME ACTIVITY; NITROGEN FIXATION; NONHUMAN; PLANT STEM; SINORHIZOBIUM MELILOTI;

ACETYL COENZYME A; BACTERIAL PROTEINS; BIOMASS; CITRATE (SI)-SYNTHASE; HYDROXYBUTYRATES; INDOLEACETIC ACIDS; KETOGLUTARATE DEHYDROGENASE COMPLEX; MEDICAGO TRUNCATULA; MICROBIAL VIABILITY; NITROGEN FIXATION; PLANT GROWTH REGULATORS; PLANT STEMS; POLYESTERS; SINORHIZOBIUM MELILOTI;

MEDICAGO TRUNCATULA; SINORHIZOBIUM MELILOTI; SINORHIZOBIUM MELILOTI 1021;

EID: 67349115248     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-009-1974-z     Document Type: Article

References (63)

1. P Allenza TG Lessie 1982 Pseudomonas cepacia mutants blocked in the Entner-Doudoroff pathway J Bacteriol 150 1340 1347 (Pubitemid 12015840)
2. A Arias C Cervenansky A Gardiol G Martinez-Drets 1979 Phosphoglucose isomerase mutant of Rhizobium meliloti J Bacteriol 137 409 414 (Pubitemid 9097586)
3. Becker A, Ruberg S (2003) Sinorhizobium 6kOligo microarray manual, V. 1.1, Department of Genetics, University of Bielefeld
4. A Becker H Bergès E Krol C Bruano S Rüberg D Capela E Lauber E Meilhoc F Ampe FJ de Bruijn J Fourment A Francez-Charlot D Kahn H Küster C Liebe A Pühler S Weidner J Batut 2004 Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions Mol Plant Microbe Interact 17 292 303 (Pubitemid 38403228)
5. C Bianco E Imperlini R Calogero B Senatore A Amoresano A Carpentieri P Pucci R Defez 2006 Indole-3-acetic acid improves Escherichia coli's defences to stress Arch Microbiol 185 373 382 (Pubitemid 43747466)
6. C Bianco E Imperlini R Calogero B Senatore P Pucci R Defez 2006 Indole-3-acetic acid regulates the central metabolic pathways in Escherichia coli Microbiology 152 2421 2431 (Pubitemid 44219648)
7. MM Bradford 1976 A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 248 254
8. Camerini S, Senatore B, Imperlini E, Bianco C, Miraglia E, Lonardo E, Defez R (2004) Improve legume yield by phytohormone release from soil bacteria. Legumes for the benefit of agriculture, nutrition and the environment. AEP, Dijon, pp 127-128
9. S Camerini B Senatore E Lonardo E Imperlini C Bianco G Moschetti GL Rotino B Campion R Defez 2008 Introduction of a novel pathway for IAA biosynthesis to rhizobia alters vetch root nodule development Arch Microbiol 190 67 77
10. MA Cevallos S Encarnacion A Leija Y Mora J Mora 1996 Genetic and physiological characterization of a Rhizobium etli mutant strain unable to synthesize poly-β-hydroxybutyrate J Bacteriol 178 1646 1654 (Pubitemid 26085613)
11. Crespi M, Frugier F (2008) De novo organ formation from differentiated cells: root nodule organogenesis. Sci Signal 1:re11
12. MP de Melo TM de Lima TC Pithon-Curi R Curi 2004 The mechanism of indole acetic acid cytotoxicity Toxicol Lett 148 103 111 (Pubitemid 38268107)
13. Defez R (2006) Patent Holder: CNR Deposited on 14/06/2005, Italian Patent Office: n. RM2005A000308. PCT extension n. PCT/IT2006/000449. Method for increasing the survival of bacterial strains of the Rhizobium genus. http://ep.espacenet.com/
14. Defez R, Spena A (1998) EPO application No. EP98/830674.2. PCT extension n° PCT24190. Method to control gene expression in bacteria, namely Rhizobiaceae, to improve root nodule development, nitrogen fixation and plant biomass production. http://ep.espacenet.com/
15. GH Dixon HL Kornberg 1969 Malate synthase from Baker's yeast Methods in Enzymol 13 633 634
16. MJ Duncan DG Fraenkel 1979 α-Ketoglutarate dehydrogenase mutant of Rhizobium meliloti J Bacteriol 137 415 419 (Pubitemid 9097587)
17. MF Dunn 1998 Tricarboxylic acid cycle and anaplerotic enzymes in rhizobia FEMS Microbiol Rev 22 105 123 (Pubitemid 28467109)
18. S Encarnacion M Dunn K Willms J Mora 1995 Fermentative and aerobic metabolism in Rhizobium etli J Bacteriol 177 3058 3066
19. F Fougere D Le Rudulier JG Streeter 1991 Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of alfalfa (Medicago sativa L.) Plant Physiol 96 1228 1236 (Pubitemid 21914153)
20. DG Fraenkel SR Levisohn 1967 Glucose and gluconate metabolism in an Escherichia coli mutant lacking phosphoglucose isomerase J Bacteriol 93 1571 1578
21. DJ Gage 2004 Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes Microbiol Mol Biol Rev 68 280 300 (Pubitemid 38756866)
22. DJ Gage T Bobo SR Long 1996 Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa) J Bacteriol 178 7159 7166 (Pubitemid 26424629)
23. F Galibert TM Finan SR Long A Puhler P Abola F Ampe F Barloy-Hubler MJ Barnett A Becker P Boistard G Bothe M Boutry L Bowser J Buhrmester E Cardieu D Capela P Chain A Cowie RW Davis S Dreano NA Federspiel RF Fisher S Gloux T Godrie A Goffeau B Golding G Gouzy M Gurjal I Hernandez-Lucas A Hong L Huizar R Hyman T Jones D Kahn ML Kahn S Kalman DH Keating E Kiss C Komp V Lelaure D Masuy C Palm M Psck TM Pohl D Potetelle B Pumelle U Ramsperger R Surzycki P Thebault M Vandenbol FJ Vorholter S Weidner DH Wells K Wong KC Yeh J Batut 2001 The composite genome of the legume symbiont Sinorhizobium meliloti Science 293 668 672 (Pubitemid 32728664)
24. A Gardiol A Arias C Cervenansky G Martinez-Drets 1982 Succinate dehydrogenase mutant of Rhizobium meliloti J Bacteriol 151 1621 1623 (Pubitemid 13230872)
25. W Grzemski JP Akowski ML Kahn 2005 Probing the Sinorhizobium meliloti-alfalfa symbiosis using temperature-sensitive and impaired-function citrate synthase mutants Mol Microbe Plant Interact 18 134 141
26. Hayat MA (2000) Principles and techniques of electron microscopy biological applications, 4th edn. Cambridge University Press. ISBN-13: 978-0521632874
27. AM Hirsch M Bang FM Ausubel 1983 Ultrastructural analysis of ineffective alfalfa nodules formed by nif: Tn5 mutants of Rhizobium meliloti J Bacteriol 155 367 380
28. PJJ Hooykaas PM Clapwicjk MP Nuti RA Schilperoort A Roersch 1977 Transfer of the Agrobacterium tumefaciens Ti plasmid to avirulent Agrobacteria and to Rhizobium ex-planta J Gen Microbiol 98 477 484 (Pubitemid 8024931)
29. JJ Irigoyen M Sanchez-Diaz DW Emerich 1990 Carbon metabolism enzymes of Rhizobium meliloti cultures and bacteroids and their distribution within the alfalfa nodule Appl Environ Microbiol 56 2587 2589 (Pubitemid 20235713)
30. HL Jensen 1942 Nitrogen fixation in leguminous plant General characters of root-nodule bacteria isolated from species of Medicago and Trifolium. Aust Proc Linn Soc 66 98 108
31. KM Jones H Kobayashi BW Davies ME Taga GC Walker 2007 How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model Nat Rev Microbiol 5 619 633 (Pubitemid 47074117)
32. BL Kittell DR Helinski GS Ditta 1989 Aromatic aminotransferase activity and indoleacetic acid production in Rhizobium meliloti J Bacteriol 171 5458 5466
33. HB Krishnan WS Kim J Sun-Hyung K Yong Kim G Jiang 2003 Citrate synthase mutants of Sinorhizobium fredii USDA257 form ineffective nodules with aberrant ultrastructure Appl Environ Microbiol 69 3561 3568 (Pubitemid 36693367)
34. JH Law RA Slepecky 1961 Assay of poly-β-hydroxybutyric acid J Bacteriol 82 33 42
35. KH Ling V Paetkau F Marcus HA Lardy 1969 Phosphofructokinase Methods Enzymol 9 425 429
36. EM Lodwing M Leonard S Marroqui TR Wheeler K Findlay JA Downie PS Poole 2005 Role of polyhydroxybutyrate and glycogen as carbon storage compounds in pea and bean bacteroids Mol Plant Microbe Interact 18 67 74 (Pubitemid 40033931)
37. TR McDermott ML Kahn 1992 Cloning and mutagenesis of the Rhizobium meliloti isocitrate dehydrogenase gene J Bacteriol 174 4790 4797
38. TR McDermott SM Griffith CP Vance PH Graham 1989 Carbon metabolism in Bradyrhizobium bacteroids FEMS Microbiol Rev 63 327 340 (Pubitemid 20002472)
39. AB McFadden 1969 Isocitrate lyase Methods in Enzymol 13 163 165
40. E Mertens 1991 Pyrophosphate-dependent phosphofructokinase, an anaerobic glycolytic enzyme? FEBS Lett 285 1 5
41. Mezzetti B, Landi L, Pandolfini T, Spena A (2004) The defH9-iaaM auxin-synthesizing gene increases plant fecundity and fruit production in strawberry and raspberry. BMC Biotechnology 4:4. Published online
42. MW Mortimer TR McDermott GM York GC Walker M Kahn 1999 Citrate synthase mutants of Sinorhizobium meliloti are ineffective and have altered cell surface polysaccharides J Bacteriol 181 7608 761
43. K Mulongoy GH Elkan 1977 Glucose catabolism in two derivatives of a Rhizobium japonicum strain differing in nitrogen-fixing efficiency J Bacteriol 131 179 187 (Pubitemid 8153476)
44. AS Paau JL Cowles 1978 Development of bacteroids in alfalfa (Medicago sativa) nodules Plant Physiol 62 526 530
45. JM Palacios J Murillo A Leyva G Ditta TR Argueso 1990 Differential expression of hydrogen uptake (hup) genes in vegetative and symbiotic cells of Rhizobium leguminosarum Mol Gen Genet 221 363 370 (Pubitemid 20195855)
46. T Pandolfini A Storlazzi E Calabria R Defez A Spena 2000 The spliceosomal intron of the rolA gene of Agrobacterium rhizogenes is a prokaryotic promoter Mol Microbiol 35 1326 1334 (Pubitemid 30175509)
47. Pandolfini T, Rotino GL, Camerini S, Defez R, Spena A (2002) Optimisation of transgene action at the post-transcriptional level: high quality parthenocarpic fruits in industrial tomatoes. BMC Biotechnology 2:1. Published online
48. Y Pii M Crimi G Cremonese A Spena T Pandolfini 2007 Auxin and nitric oxide control indeterminate nodule formation BMC Plant Biol 7 21
49. P Poole D Allaway 2000 Carbon and nitrogen metabolism in Rhizobium Adv Microb Physiol 43 117 163 (Pubitemid 30481124)
50. S Povolo S Casella 2000 A critical role for aniA in energy-carbon flux and symbiotic nitrogen fixation in Sinorhizobium meliloti Arch Microbiol 174 42 49 (Pubitemid 30625679)
51. R Prusty P Grisafi GR Fink 2004 The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae Proc Natl Acad Sci U S A 101 4153 4157 (Pubitemid 38405898)
52. LJ Reed BB Mukherjee 1969 α-Ketoglutarate dehydrogenase complex from Escherichia coli Methods Enzymol 13 55 61
53. SO Salminen JG Streeter 1990 Factors contributing to the accumulation of glutamate in Bradyrhizobium japonicum bacteroids under microaerobic conditions J Gen Microbiol 136 2119 2126 (Pubitemid 20350976)
54. W Saubert H Weicker 1969 Pyruvate carboxylase from Pseudomonas Methods Enzymol 13 258 262
55. PJ Senior EA Dawes 1973 The regulation of poly-β-hydroxybutyrate metabolism in Azotobacter beijerinckii Biochem J 134 225 238
56. GK Smyth TP Speed 2003 Normalization of cDNA microarray data Methods 31 265 273 (Pubitemid 37338763)
57. GK Smyth J Michaud H Scott 2005 The use of within-array replicate spots for assessing differential expression in microarray experiments Bioinformatics 21 2067 2075 (Pubitemid 40668046)
58. S Spaepen J Vanderleyden R Remans 2007 Indole-3-acetic acid in microbial and microorganism-plant signaling FEMS Microbiol Rev 31 425 448 (Pubitemid 46920250)
59. MD Stowers 1985 Carbon metabolism in Rhizobium species Annu Rev Microbiol 39 89 108
60. JE Urban FB Dazzo 1982 Succinate-induced morphology of Rhizobium trifolii 0403 resembles that of bacteroids in clover nodules Appl Environ Microbiol 44 219 226 (Pubitemid 12068786)
61. J Vasse F de Billy S Camut G Truchet 1990 Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules J Bacteriol 172 4295 4306 (Pubitemid 20236718)
62. D Walshaw A Wilkinson M Mundy M Smith PS Poole 1997 Regulation of the TCA cycle and the general amino acid permease by overflow metabolism in Rhizobium leguminosarum Microbiology 143 2209 2221 (Pubitemid 27356755)
63. PDJ Weitzman 1969 Citrate synthase from Escherichia coli Methods Enzymol 13 22 26