The contribution of bacteroidal nitrate and nitrite reduction to the formation of nitrosylleghaemoglobin complexes in soybean root nodules Free

Abstract

It is becoming recognized that leghaemoglobin constitutes an important buffer for the cytotoxic nitric oxide radical (NO) in root nodules, although the sources of this NO within nodules are unclear. In bacteroids, NO can be produced through the denitrification process, during which nitrate is reduced to nitrite by the periplasmic nitrate reductase Nap, and nitrite is reduced to NO by the respiratory nitrite reductase NirK. To assess the contribution of bacteroidal denitrification to the NO within nitrate-treated soybean nodules, electron paramagnetic resonance and UV–visible spectroscopy were employed to study the presence of nitrosylleghaemoglobin (LbNO) within nodules from plants inoculated with wild-type, or strains. Since it has been found that hypoxia induces NO production in plant root tissue, and that plant roots can be subjected to hypoxic stress during drought and flooding, the effect of hypoxic stress on the formation of LbNO complexes within nodules was also investigated. Maximal levels of LbNO were observed in nodules from plants treated with nitrate and subjected to hypoxic conditions. It is shown that, in the presence of nitrate, all of the LbNO within normoxic nodules arises from nitrate reduction by the bacteroidal periplasmic nitrate reductase, whereas Nap activity is only responsible for half of the LbNO within hypoxic nodules. In contrast to Nap, NirK is not essential for LbNO formation under any condition tested.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/000059-0
2007-02-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/2/411.html?itemId=/content/journal/micro/10.1099/mic.0.2006/000059-0&mimeType=html&fmt=ahah

References

  1. Allegre A., Silvestre J., Morard P., Kallerhoff J., Pinelli E. 2004; Nitrate reductase regulation in tomato roots by exogenous nitrate: a possible role in tolerance to long-term root anoxia. J Exp Bot 55:2625–2634 [CrossRef]
    [Google Scholar]
  2. Appleby C. A. 1992; The origin and functions of hemoglobin in plants. Sci Progress 76:365–398
    [Google Scholar]
  3. Baudouin E., Pleuchot L., Engler G., Pauly N., Puppo A. 2006; Nitric oxide is formed in Medicago truncatula–Sinorhizobium meliloti functional nodules. Mol Plant Microbe Interact 19:970–975 [CrossRef]
    [Google Scholar]
  4. Blumwald E., Fortin M. G., Rea P. A., Verma D. P. A., Roole R. J. 1985; Presence of host-plasma membrane type H+-ATPase in the membrane envelope enclosing the bacteroids in soybean root nodules. Plant Physiol 78:665–672 [CrossRef]
    [Google Scholar]
  5. Butler C. S., Charnock J. M., Bennett B., Sears H. J., Reilly A. J., Ferguson S. J., Garner C. D., Lowe D. J., Thomson A. J. other authors 1999; Models for molybdenum co-ordination during the catalytic cycle of periplasmic nitrate reductase from Paracoccus denitrificans derived from EPR and EXAFS spectroscopy. Biochemistry 38:9000–9012 [CrossRef]
    [Google Scholar]
  6. Cueto M., Bentura M. L., Rodigo J., Lamas S., Golvano M. P., Hernández-Perera O., Martín R. 1996; Presence of nitric oxide synthase activity in roots and nodules of Lupinus albus . FEBS Lett 398:159–164 [CrossRef]
    [Google Scholar]
  7. Delgado M. J., Bedmar E. J., Downie J. A. 1998; Genes involved in the formation and assembly of rhizobial cytochromes and their role in symbiotic nitrogen fixation. Adv Microbial Phys 40:191–231
    [Google Scholar]
  8. Delgado M. J., Bonnard N., Tresierra-Ayala A., Bedmar E. J., Müller P. 2003; The Bradyrhizobium japonicum napEDABC genes encoding the periplasmic nitrate reductase are essential for nitrate respiration. Microbiology 149:3395–3403 [CrossRef]
    [Google Scholar]
  9. Dordas C., Hasinoff B. B., Igamberdiev A. U., Manach N., Rivoal J., Hill R. D. 2003; Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J 35:763–770 [CrossRef]
    [Google Scholar]
  10. Dordas C., Hasinoff B. B., Rivoal J., Hill R. D. 2004; Class-1 hemoglobins, nitrate and NO levels in anoxic maize cell-suspension cultures. Planta 219:66–72 [CrossRef]
    [Google Scholar]
  11. Fenner B. J., Tiwari R. P., Reeve W. G., Dilworth M. J., Glenn A. R. 2004; Sinorhizobium medicae gene whose regulation involves the ActS and/or ActR signal transduction proteins. FEMS Microbiol Lett 236:21–31 [CrossRef]
    [Google Scholar]
  12. Glaab J., Kaiser W. M. 1993; Rapid modulation of nitrate reductase in pea roots. Planta 191:173–179
    [Google Scholar]
  13. Guo F.-Q., Okamoto M., Crawford N. M. 2003; Identification of a plant nitric oxide synthase gene involved in hormonal signalling. Science 302:100–103 [CrossRef]
    [Google Scholar]
  14. Gupta K. J., Stoimenova M., Kaiser W. M. 2005; In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ . J Exp Bot 56:2601–2609 [CrossRef]
    [Google Scholar]
  15. Haaker H. 1988; Biochemistry and physiology of nitrogen fixation. BioEssays 9:112–117 [CrossRef]
    [Google Scholar]
  16. Herold S., Puppo A. 2005; Oxyleghaemoglobin scavenges nitrogen monoxide and peroxynitrite: a possible role in functioning nodules?. J Biol Inorg Chem 10:935–945 [CrossRef]
    [Google Scholar]
  17. Jepson B., Anderson L., Rubio L., Taylor C., Butler C., Herrero A., Flores E., Butt J. N., Richardson D. J. 2004; Tuning a nitrate reductase for function: the first spectropotentiometric characterization of a bacterial assimilatory nitrate reductase reveals novel redox properties. J Biol Chem 279:32212–32218 [CrossRef]
    [Google Scholar]
  18. Jones D. K., Badii R., Rosell F. I., Lloyd E. 1998; Bacterial expression and spectroscopic characterization of soybean leghaemoglobin a. Biochem J 330:983–988
    [Google Scholar]
  19. Kanayama Y., Yamamoto Y. 1990a; Inhibition of nitrogen fixation in soybean plants supplied with nitrate II. Accumulation and properties of nitrosylleghaemoglobin in nodules. Plant Cell Physiol 31:207–214
    [Google Scholar]
  20. Kanayama Y., Yamamoto Y. 1990b; Inhibition of nitrogen fixation in soybean plants supplied with nitrate III. Kinetics of the formation of nitrosylleghaemoglobin and of the inhibition of formation of oxyleghaemoglobin. Plant Cell Physiol 31:603–608
    [Google Scholar]
  21. Kanayama Y., Watanabe I., Yamamoto Y. 1990; Inhibition of nitrogen fixation in soybean plants supplied with nitrate I. Nitrite accumulation and formation of nitrosylleghaemoglobin in nodules. Plant Cell Physiol 31:341–346
    [Google Scholar]
  22. Kaneko T., Nakamura Y., Sato S., Minamisawa K., Ughiuma T., Sasamoto S., Watanabe A., Idesawa K., Iriguchi M. other authors 2002; Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9:189–197 [CrossRef]
    [Google Scholar]
  23. Lamotte O., Courtois C., Barnavon L., Pugin A., Wendehenne D. 2005; Nitric oxide in plants: the biosynthesis and cell signalling properties of a fascinating molecule. Planta 221:1–4 [CrossRef]
    [Google Scholar]
  24. Lin J. T., Stewart V. 1998; Nitrate assimilation by bacteria. Adv Microb Physiol 39:1–30
    [Google Scholar]
  25. Linkemer G., Board J. E., Musgrave M. E. 1998; Waterlogging effects on growth and yield components in late-planted soybean. Crop Sci 38:1576–1584 [CrossRef]
    [Google Scholar]
  26. Mathieu C., Moreau S., Frendo P., Puppo A., Davies M. J. 1998; Direct detection of radicals in intact soybean nodules: presence of nitric oxide–leghaemoglobin complexes. Free Radic Biol Med 24:1242–1249 [CrossRef]
    [Google Scholar]
  27. Mesa S., Velasco L., Manzanera M. E., Delgado M. J., Bedmar E. J. 2002; Characterisation of the norBCQD genes, encoding nitric oxide reductase, in the nitrogen fixing bacterium Bradyrhizobium japonicum . Microbiology 148:3553–3560
    [Google Scholar]
  28. Mesa S., Bedmar E. J., Chanfon A., Hennecke H., Fischer H.-M. 2003; Bradyrhizobium japonicum NnrR, a denitrification regulator, expands the FixLJ–FixK2 regulatory cascade. J Bacteriol 185:3978–3982 [CrossRef]
    [Google Scholar]
  29. Mesa S., Bedmar E. J., Delgado M. J., de Dios Alché J. 2004; Expression of the nir , nor and nos denitrification genes from Bradyrhizobium japonicum in soybean root nodules. Physiol Plant 120:205–211 [CrossRef]
    [Google Scholar]
  30. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  31. Minchin F. R. 1997; Regulation of oxygen diffusion in legume nodules. Soil Biol Biochem 29:881–888 [CrossRef]
    [Google Scholar]
  32. Nicholas D. J. D., Nason A. 1957; Determination of nitrate and nitrite. In Methods in Enzymology pp 981–984 Edited by Colowick S. P., Kaplan N. O. New York: Academic Press;
    [Google Scholar]
  33. Preisig O., Zufferey R., Appleby C. A., Hennecke H., Thöny-Meyer L. 1996; A high-affinity cbb 3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum . J Bacteriol 178:1532–1538
    [Google Scholar]
  34. Regensburger B., Hennecke H. 1983; RNA polymerase from Rhizobium japonicum . Arch Microbiol 135:103–109 [CrossRef]
    [Google Scholar]
  35. Rigaud J., Puppo A. 1975; Indole-3-acetic acid catabolism by soybean bacteroids. J Gen Microbiol 88:223–228 [CrossRef]
    [Google Scholar]
  36. Robles E. F., Delgado M. J., Bedmar E. J., Sánchez C. 2006; The Bradyrhizobium japonicum napEDABC genes are controlled by the FixLJ-FixK2-NnrR regulatory cascade. Biochem Soc Trans 34:108–110 [CrossRef]
    [Google Scholar]
  37. Velasco L., Mesa S., Delgado M. J., Bedmar E. J. 2001; Characterization of the nirK gene encoding the respiratory, Cu-containing nitrite reductase of Bradyrhizobium japonicum . Biochim Biophys Acta 1521130–134 [CrossRef]
    [Google Scholar]
  38. Velasco L., Mesa S., Xu C., Delgado M. J., Bedmar E. J. 2004; Molecular characterization of nosRZDFYLX genes coding for denitrifying nitrous oxide reductase of Bradyrhizobium japonicum . Antonie van Leeuwenhoek 85:229–235 [CrossRef]
    [Google Scholar]
  39. Yamasaki H., Sakihama S. 2000; Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 468:89–92 [CrossRef]
    [Google Scholar]
  40. Yamasaki H., Sakihama Y., Takahashi S. 1999; An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci 4:128–129 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/000059-0
Loading
/content/journal/micro/10.1099/mic.0.2006/000059-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed