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PMID: 15007732 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Sinorhizobium meliloti RpoH1 is required for effective nitrogen-fixing symbiosis with alfalfa.

Molecular genetics and genomics : MGG ·Vol. 271 ·No. 4 ·2004-05-00 ·Pages 416-25

Mitsui H, Sato T, Sato Y, Ito N, Minamisawa K

Abstract

Sinorhizobium meliloti is a root-nodulating, nitrogen-fixing bacterium. An S. meliloti strain that is mutant for the rpoH(1) gene, which encodes a sigma(32)-like protein, elicits the formation of ineffective nodules on the host plant alfalfa. We characterized the rpoH(1) mutant for phenotypes related to symbiosis. Alfalfa nodules formed by the rpoH(1) mutant exhibited greatly reduced levels of acetylene reduction activity compared to the wild-type nodules. Whereas intracellular colonization by rhizobia was observed in a zone just below the apical meristem, we found ultrastructural abnormalities and signs of degeneration of bacteroids within many host cells in the proximally adjacent zone. In the proximal part of the nodule, only a few nodule cells contained bacteroids. In contrast, the rpoH(1) mutant showed normal induction of nitrogen fixation gene expression in microaerobic culture. These results suggest that the rpoH(1) mutation causes early senescence of bacteroids during the endosymbiotic process, but does not affect the invasion process or the synthesis of the nitrogenase machinery. The rpoH(1) mutant exhibited increased sensitivity to various agents and to acid pH, suggesting that RpoH(1) is required to protect the bacterial cell against environmental stresses encountered within the host. Since RpoH(1) was previously reported to be required for the synthesis of some heat shock proteins (Hsps), we examined the transcription of several genes for Hsp homologs. We found that transcription of groESL(5), lon, and clpB after heat shock was RpoH(1)-dependent, and conserved nucleotide sequences were found in the -35 and -10 regions upstream of the transcription start sites of these genes. Although groESL(5) expression is almost completely dependent on RpoH(1), we found that a groESL(5) mutant strain is still capable of normal symbiotic nitrogen fixation on alfalfa.

MeSH Terms
Base Sequence Heat-Shock Proteins/physiology Medicago sativa/physiology Molecular Sequence Data Nitrogen Fixation Sigma Factor/chemistry,genetics,metabolism,physiology Sinorhizobium meliloti/chemistry Symbiosis
Chemicals
Heat-Shock Proteins Sigma Factor heat-shock sigma factor 32
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Mitsui H
Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, 980-8577 Sendai, Japan. hmitsui@ige.tohoku.ac.jp
Sato T
Sato Y
Ito N
Minamisawa K
References (32)
32 references, click to expand
  1. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum.
    Gene. 1994 Jul 22;145(1):69-73 PMID: 8045426
  2. Molecular characterization of Tn5-induced symbiotic (Fix-) mutants of Rhizobium meliloti.
    J Bacteriol. 1983 Dec;156(3):1025-34 PMID: 6196347
  3. Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules.
    J Bacteriol. 1990 Aug;172(8):4295-306 PMID: 2376562
  4. Two RpoH homologs responsible for the expression of heat shock protein genes in Sinorhizobium meliloti.
    Mol Gen Genet. 2001 Feb;264(6):902-12 PMID: 11254138
  5. Transcriptome analysis of Sinorhizobium meliloti during symbiosis.
    Genome Biol. 2003;4(2):R15 PMID: 12620125
  6. The ++Sinorhizobium meliloti lon protease is involved in regulating exopolysaccharide synthesis and is required for nodulation of alfalfa.
    J Bacteriol. 2000 May;182(9):2551-8 PMID: 10762258
  7. Outer penetration barrier of Escherichia coli K-12: kinetics of the uptake of gentian violet by wild type and envelope mutants.
    J Bacteriol. 1973 Nov;116(2):893-900 PMID: 4583255
  8. Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules.
    Proc Natl Acad Sci U S A. 1985 Sep;82(18):6231-5 PMID: 3862129
  9. Effects of Rhizobium meliloti nif and fix mutants on alfalfa root nodule development.
    J Bacteriol. 1987 Mar;169(3):1137-46 PMID: 3818542
  10. Genetic techniques in Rhizobium meliloti.
    Methods Enzymol. 1991;204:398-418 PMID: 1658566
  11. Cascade regulation of nif gene expression in Rhizobium meliloti.
    Cell. 1988 Aug 26;54(5):671-83 PMID: 2842062
  12. Nodulation of legumes by members of the beta-subclass of Proteobacteria.
    Nature. 2001 Jun 21;411(6840):948-50 PMID: 11418858
  13. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti.
    DNA Res. 2000 Dec 31;7(6):331-8 PMID: 11214968
  14. Identification of the heat-shock sigma factor RpoH and a second RpoH-like protein in Sinorhizobium meliloti.
    Microbiology. 2001 Sep;147(Pt 9):2399-408 PMID: 11535780
  15. Deficiency of a Sinorhizobium meliloti BacA mutant in alfalfa symbiosis correlates with alteration of the cell envelope.
    J Bacteriol. 2002 Oct;184(20):5625-32 PMID: 12270820
  16. Heat shock protein GroE of Escherichia coli: key protective roles against thermal stress.
    Genes Dev. 1988 Jul;2(7):874-82 PMID: 2905317
  17. Deletion analysis of Rhizobium meliloti symbiotic promoters.
    EMBO J. 1985 Oct;4(10):2419-24 PMID: 15929217
  18. Genetic regulation of nitrogen fixation in rhizobia.
    Microbiol Rev. 1994 Sep;58(3):352-86 PMID: 7968919
  19. Effects of organic acids and low pH on Rhizobium meliloti 104A14.
    Microbiology. 1994 May;140 ( Pt 5):1231-5 PMID: 8025689
  20. Chronic intracellular infection of alfalfa nodules by Sinorhizobium meliloti requires correct lipopolysaccharide core.
    Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3938-43 PMID: 11904442
  21. Rhizobium meliloti ntrA (rpoN) gene is required for diverse metabolic functions.
    J Bacteriol. 1987 Jun;169(6):2424-31 PMID: 3034856
  22. The composite genome of the legume symbiont Sinorhizobium meliloti.
    Science. 2001 Jul 27;293(5530):668-72 PMID: 11474104
  23. New gentamicin-resistance and lacZ promoter-probe cassettes suitable for insertion mutagenesis and generation of transcriptional fusions.
    Gene. 1995 Aug 30;162(1):37-9 PMID: 7557413
  24. Differential and independent roles of a sigma(32) homolog (RpoH) and an HrcA repressor in the heat shock response of Agrobacterium tumefaciens.
    J Bacteriol. 1999 Dec;181(24):7509-15 PMID: 10601208
  25. A Rhizobium meliloti lipopolysaccharide mutant altered in competitiveness for nodulation of alfalfa.
    J Bacteriol. 1992 Sep;174(18):5941-52 PMID: 1325969
  26. The Bradyrhizobium japonicum rpoH1 gene encoding a sigma 32-like protein is part of a unique heat shock gene cluster together with groESL1 and three small heat shock genes.
    J Bacteriol. 1996 Sep;178(18):5337-46 PMID: 8808920
  27. Ultrastructural analysis of ineffective alfalfa nodules formed by nif::Tn5 mutants of Rhizobium meliloti.
    J Bacteriol. 1983 Jul;155(1):367-80 PMID: 6575011
  28. Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis.
    J Bacteriol. 1982 Jan;149(1):114-22 PMID: 6274841
  29. Three disparately regulated genes for sigma 32-like transcription factors in Bradyrhizobium japonicum.
    Mol Microbiol. 1997 Apr;24(1):93-104 PMID: 9140968
  30. Plasmids related to the broad host range vector, pRK290, useful for gene cloning and for monitoring gene expression.
    Plasmid. 1985 Mar;13(2):149-53 PMID: 2987994
  31. Heat shock activation of the groESL operon of Agrobacterium tumefaciens and the regulatory roles of the inverted repeat.
    J Bacteriol. 1996 Jun;178(12):3634-40 PMID: 8655565
  32. Mutation in the ntrR gene, a member of the vap gene family, increases the symbiotic efficiency of Sinorhizobium meliloti.
    Mol Plant Microbe Interact. 2001 Jul;14(7):887-94 PMID: 11437262
Article Info
Journal
Molecular genetics and genomics : MGG
Abbr.
Mol Genet Genomics
ISSN
1617-4615
Published
2004-05-00
Epub
2004-00-06
Pages
416-25
Language
English
Region
Germany
NLM ID
101093320
Subset
IM
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