Comparative cytochemical analysis of hydrogen peroxide distribution in pea ineffective mutant SGEFix--1 (sym40) and initial line SGE



Cite item

Full Text

Abstract

Comparative cytochemical analysis has revealed differences in hydrogen peroxide distribution in symbiotic nodules of pea initial line SGE and mutant SGEFix--1 (sym40). In the initial line SGE, precipitates of cerium perhydroxide were deposited in the walls of infection threads and in adjacent material in the luminal matrix. In mutant SGEFix--1, an increased deposition of cerium perhydroxide precipitates was observed in the matrix of hypertrophied infection droplets, round bacteria contained in infection threads and also around juvenile bacteroids. The observed pattern of hydrogen peroxide distribution indicates that bacteria in infected cells of mutant nodules are exposed to a stronger oxidative stress compared with nodules of the initial line.

About the authors

Anna V Tsyganova

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Email: anna_khodorenko@arriam.spb.ru Podbelskiy Ch., 3, Saint-Petersburg, Pushkin-8, 196608, Russ

Viktor E Tsyganov

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Email: viktor_tsyganov@arriam.spb.ru

Aleksey U Borisov

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Email: ayborisov@yandex.ru

Igor A Tikhonovich

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Email: arriam@arriam.spb.ru. contact@arriam.spb.ru Podbelskiy Ch., 3, Saint-Petersburg, Pushkin-8

Nicholas Brewin

The John Innes Centre, Norwich, UK

Email: nick.brewin@bbsrc.ac.uk NR4 7UH, Colney Lane, Norwich, United Kingdom

References

  1. Alesandrini F., Mathis R., Van de Sype G. et al. Possible roles for a cysteine protease and hydrogen peroxide in soybean nodule development and senescence//New Phytol. 2003. Vol. 158. P. 131 -138.
  2. Appleby C.A. Leghemoglobin and Rhizobium respiration//Ann. Rev. Plant Physiol. 1984. Vol. 35. P 443-478.
  3. Becana M., Dalton D. A., Moran J. F. et al. Reactive oxygen species and antioxidants in legume nodules//Physiol. Plant. 2000. Vol. 109. P. 372-381.
  4. Bestwick C. S., Brown I. R, Bennett M. R., Mansfield J. W. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola//Plant Cell. 1997. Vol. 9. P. 209-221.
  5. Borisov A. Y., Rozov S. M., Tsyganov V. E. et al. Sequential functioning of Sym 13 and Sym 31, two genes affecting symbiosome development in root nodules of pea (Pisum sativum L.)//Mol. Gen. Genet. 1997. Vol. 254. P. 592-598.
  6. Brewin N.J. Development of the legume root nodule//Annu. Rev. Cell Biol. 1991. Vol. 7. P. 191-226.
  7. Brewin N. J. Plant cell wall remodelling in the Rhizobium-legume symbiosis//Critic. Rev. Plant Sci. 2004. Vol. 23. P. 293-316.
  8. D'Haeze W., DeRycke R., Mathis R. et al. Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume//Proc. Natl. Acad. Sci. USA. 2003. Vol. 100. P 11789-11794.
  9. Dalton D. A., Baird L. M., Langeberg L. et al. Subcellular localization of oxygen defense enzymes in soybean (Glycine max [L.] Merr.) root nodules//Plant Physiol. 1993. Vol. 102. P. 481-489.
  10. Dalton D. A., Russel S. A., Hanus F. J. et al. Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules//Proc. Natl. Acad. Sci. USA. 1986. Vol. 83. P. 381 1-3815.
  11. Dombrecht B., Heusdens C., Beullens S. et al. Defence of Rhizobium etli bacteroids against oxidative stress involves a complexly regulated atypical 2-Cys peroxiredoxin//Mol. Microbiol. 2005. Vol. 55. P. 1207-1221.
  12. Evans P. J., Gallesi D., Mathieu C. et al. Oxidative stress occurs during soybean nodule senescence//Planta. 1999. Vol. 208. P. 73-79.
  13. Groten K., Vanacker H., Duttileul C. et al. The roles of redox processes in pea nodule development and senescence//Plant Cell Environ. 2005. Vol. 28. P. 1293-1304.
  14. Hancock J. T., Desikan R., Clarke A. et al. Cell signalling following plant/pathogen interactions involves the generation of reactive oxygen and reactive nitrogen species//Plant Physiol. Biochem. 2002. Vol. 40. P. 611-617.
  15. Harrison J., Jamet A., Muglia C. I. et al. Glutathione plays a fundamental role in growth and symbiotic capacity of Sinorhizobium meliloti//J. Bacteriol. 2005. Vol. 187, N 1. P. 168-174.
  16. Herouart D., Baudouin E., Frendo P. et al. Reactive oxygen species, nitric oxide and glutathione: a key role in the establishment of the legume-Rhizobium symbiosis?//Plant Physiol. Biochem. 2002. Vol. 40. P. 619-624.
  17. Herouart D., Sigaud S., Moreau S. et al. Cloning and characterization of the katA gene of Rhizobium meliloti encoding a hydrogen peroxide-inducible catalase//J. Bacteriol. 1996. Vol. 178, N 23. P. 6802-6809.
  18. Imlay J. A. How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis//Adv. Microb. Physiol. 2002. Vol. 46. P. 111 -153.
  19. Imlay J. A. Pathways of oxidative damage//Annu. Rev. Microbiol. 2003. Vol. 57. P. 395-418.
  20. Jamet A., Sigaud S., Van de Sype G. et al. Expression of the bacterial catalase genes during Sinorhizobium meliloti-Medicago sativa symbiosis and their crucial role during the infection process//Mol. Plant Microbe Interact. 2003. Vol. 16. P. 217-225.
  21. Kawashima K., Suganuma N., Tamaoki M., Kouchi H. Two types of pea leghemoglobin genes showing different O2-binding affinities and distinct patterns of spatial expression in nodules//Plant Physiol. 2001. Vol. 125. P. 641-651.
  22. Kosterin O. E., Rozov S. M. Mapping of the new mutation blb and the problem of integrity of linkage group I//Pisum Genet. 1993. Vol. 25. P. 27-31.
  23. Lamb C., Dixon R. A. The oxidative burst in plant disease resistance//Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997. Vol. 48. P. 251-275.
  24. Matamoros M. A., Dalton D. A., Ramos J. et al. Biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis//Plant Physiol. 2003. Vol. 133. P. 499-509.
  25. Mathieu C., Moreau S., Frendo P. et al. Direct detection of radicals in intact soybean nodules: presence of nitric oxide-leghemoglobin complexes//Free Rad. Biol. Med. 1998. Vol. 24. P. 1242-1249.
  26. Minchin F. R., James E. K., Becana M. Oxygen diffusion, production of reactive oxygen and nitrogen species, and antioxidants in legume nodules//Nitrogen-fixing Leguminous Symbioses/M. J. Dilworth et al. (eds.). Springer Science, Business Media B. V., 2008. P. 321-362.
  27. Ohwada T., Shirakawa Y., Kusumoto M. et al. Susceptibility to hydrogen peroxide and catalase activity of root nodule bacteria//Biosci. Biotechnol. Biochem. 1999. Vol. 63, N 3. P. 457-462.
  28. Oldroyd G. E. D., Downie J. A. Coordinating nodule morphogenesis with rhizobial infection in legumes//Annu. Rev. Plant Biol. 2008. Vol. 59. P. 519-546.
  29. Panek H. R., OBrian M. R. KatG is the primary detoxifier of hydrogen peroxide produced by aerobic metabolism in Bradyrhizobium japonicum//J. Bacteriol. 2004. Vol. 186, N 23. P. 7874-7880.
  30. Puppo A., Groten K., Bastian F. et al. Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process//New Phytol. 2005. Vol. 165. P. 683-701.
  31. Robson R. L., Postgate J. R. Oxygen and hydrogen in biological nitrogen fixation//Annu. Rev. Microbiol. 1980. Vol. 34. P. 183-207.
  32. Rubio M. C., Gonzalez E. M., Minchin F. R. et al. Effects of water stress on antioxidant enzymes of leaves and nodules of transgenic alfalfa overexpressing superoxide dismutases//Physiol. Plant. 2002. Vol. 115. P. 531-540.
  33. Rubio M. C., James E. K., Clemente M. R. et al. Localization of superoxide dismutases and hydrogen peroxide in legume root nodules//Mol. Plant Microbe Interact. 2004. Vol. 17, N 12. P. 1294-1305.
  34. Safronova V. I., Novikova N. I. Сomparison of two methods for root nodule bacteria preservation: lyophilization and liquid nitrogen freezing//J. Microbiol. Methods. 1996. Vol. 24. P. 231-237.
  35. Santos R., Bocquet S., Puppo A., Touati D. Characterization of an atypical superoxide dismutase from Sinorhizobium meliloti//J. Bacteriol. 1999. Vol. 181, N 15. P. 4509-4516.
  36. Santos R., Herouart D., Puppo A., Touati D. Critical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis//Mol. Microbiol. 2000. Vol. 38. P. 750-759.
  37. Santos R., Herouart D., Sigaud S. et al. Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction//Mol. Plant Microbe Interact. 2001. Vol. 14. P. 86-89.
  38. Schultze M., Kondorosi A. Regulation of symbiotic root nodule development//Annu. Rev. Genet. 1998. Vol. 32. P. 33-57.
  39. Sigaud S., Becquet V., Frendo P. et al. Differential regulation of two divergent Sinorhizobium meliloti genes for HPII-like catalases during free living growth and protective role of both catalases during symbiosis//J. Bacteriol. 1999. Vol. 181, N 8. P. 2634-2639.
  40. Tsyganov V. E., Morzhina E. V., Stefanov S. Y. et al. The pea (Pisum sativum L.) genes sym33 and sym40 control infection thread formation and root nodule functioning//Mol. Gen. Genet. 1998. Vol. 259. P. 491-503.
  41. Wisniewski J. P., Rathbun E. A., Knox J. P., Brewin N. J. Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implications for pea nodule initiation by Rhizobium leguminosarum//Mol. Plant Microbe Interact. 2000. Vol. 13, N 4. P. 413-420.

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2009 Tsyganova A.V., Tsyganov V.E., Borisov A.U., Tikhonovich I.A., Brewin N.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 65617 от 04.05.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies