Plant and Soil

, Volume 149, Issue 1, pp 95–102 | Cite as

Effects of high temperature on nodulation and nitrogen fixation by Phaseolus vulgaris L.

  • Mariangela Hungria
  • Avílio Antônio Franco
Research Article


Screening of Rhizobium leguminosarum bv. phaseoli strains showed some that were able to nodulate common beans (Phaseolus vulgaris L.) at high temperatures (35 and 38°C/8 h/day). The nodulation ability was not related to the capability to grow or produce melanin-like pigment in culture media at high temperatures. However, nodules formed at high temperatures were ineffective and plants did not accumulate N in shoots. Two thermal shocks of 40°C/8 h/day at flowering time drastically decreased nitrogenase activity and nodule relative efficiency of plants otherwise grown at 28°C. Recovery of nitrogenase activity began only after seven days, when new nodules formed; total incorporation of N in tops did not recover for 2 weeks. Non-inoculated beans receiving mineral N were not affected by the thermal shock, and when growing continuously at 35 or 38°C had total N accumulated in shoots reduced by only 18%.

Key words

common bean nitrogenase nodule senescence Rhizobium 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Barrios S, Raggio N and Raggio M 1963 Effect of temperature on infection of isolated bean roots by rhizobia. Plant Physiol. 38, 178–174.Google Scholar
  2. Beringer J E 1974 R factor, transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84, 188–198.PubMedGoogle Scholar
  3. Beynon J L, Beringer J E and Johnston A W B 1980 Plasmids and host-range in Rhizobium leguminosarum and Rhizobium phaseoli. J. Gen. Microbiol. 120, 421–429.Google Scholar
  4. Boddey R M, Pereira J A R, Hungria M, Thomas R J and Neves M C P 1987 Methods for the study of nitrogen assimilation and transport in grain legumes. MIRCEN J. Appl. Environm. Biotechnol. 3, 3–22.CrossRefGoogle Scholar
  5. Borthakur D, Lamb J W and Johnston A W B 1987 Identification of two classes of Rhizobium phaseoli genes required for melanin synthesis, one of which is required for nitrogen fixation and activates the transcription of the other. Mol. Gen. Genet. 207, 155–160.PubMedCrossRefGoogle Scholar
  6. Dart P J, Day J, Islam R and Döbereiner J 1976 Symbiosis in tropical grain legumes: some effects of temperature and the composition of the rooting medium. In Symbiotic Nitrogen Fixation in Plants. Ed. P SNutman. pp 361–383. Cambridge University Press. Cambridge.Google Scholar
  7. Dart P J and Mercer F V 1965 The effect of growth temperature, level of ammonium nitrate, and light intensity on the growth and nodulation of cowpea (Vigna sinensis Endl. ex. Hassk.). Aust. J. Agric. Res. 16, 321–345.CrossRefGoogle Scholar
  8. Dennet M D 1984 The tropical environment. In The Physiology of Tropical Field Crops, Eds. R PGoldsworthy and N MFisher. pp 1–38. Wiley, New York.Google Scholar
  9. Frings J F J 1976 The Rhizobium-Pea Symbiosis as Affected by High Temperatures. Thesis. Wageningen Agricultural University, Wageningen. 76 p.Google Scholar
  10. Gitonga N M, Widdowson D and Keya S O 1989 Interaction of Phaseolus vulgaris with thermotolerant isclates of Rhizobium leguminosarum biovar phaseoli from Kenyan soils. MIRCEN J. 5, 493–504.CrossRefGoogle Scholar
  11. Graham P H and Halliday J 1977 Inoculation and nitrogen fixation in the genus Phaseolus. In Exploiting the Legume Symbiosis in Tropical Agriculture. Eds. J MVincent, A SWhitney and JBose. pp 313–333. College of Tropical Agriculture Publication, 145. University of Hawaii, Hawaii, HI.Google Scholar
  12. Hernandez-Armenta R, Wien H C and Eaglesham A R J 1989 Carbohydrate partitioning and nodule functioning in common bean after heat stress. Crop Sci. 29, 1292–1297.CrossRefGoogle Scholar
  13. Hungria M, Franco A A and Sprent J I 1993 New sources of high-temperature tolerant rhizobia for Phaseolus vulgaris. Plant and Soil 149, 103–109.Google Scholar
  14. Hungria M and Neves M C P 1987a Cultivar and Rhizobium strain effects on nitrogen fixation and transport in Phaseolus vulgaris L. Plant and Soil 103, 111–121.CrossRefGoogle Scholar
  15. Hungria M and Neves M C P 1987b Partitioning of nitrogen from biological fixation and fertilizer in Phaseolus vulgaris L. Physiol. Plant. 69, 55–63.CrossRefGoogle Scholar
  16. Hynes M F, Brucksch K and Priefer U 1988 Melanin production encoded by a cryptic plasmid in a Rhizobium leguminosarum strain. Arch. Microb. 150, 326–332.CrossRefGoogle Scholar
  17. Jones F R and Tisdale W B 1921 Effect of soil temperature upon the development of nodules on the roots of certain legumes. J. Agric. Res. 22, 17–37.Google Scholar
  18. Karanja N K and Wood M 1988 Selecting Rhizobium phaseoli strains for use with beans (Phaseolus vulgaris L.) in Kenya: Tolerance of high temperature and antibiotic resistance. Plant and Soil 112, 15–22.CrossRefGoogle Scholar
  19. LaFavre A K and Eaglesham A R J 1986 The effects of high temperatures on soybean nodulation and growth with different strains of bradyrhizobia. Can. J. Microbiol. 32, 22–27.Google Scholar
  20. Lamb J W, Hombrecher G and Johnston A W B 1982 Plasmid-determined nodulation and nitrogen-fixation abilities in Rhizobium phaseoli. Mol. Gen. Genet. 186, 449–452.CrossRefGoogle Scholar
  21. Lie T A 1981 Environmental physiology of the legume-Rhizobium symbiosis. In Nitrogen Fixation. Vol I. Ed. W JBroughton. pp 104–134. Clarendon Press, Oxford.Google Scholar
  22. Meyer D R and Anderson A J 1959 Temperature and symbiotic nitrogen fixation. Nature 183, 161.CrossRefGoogle Scholar
  23. Minchin F R, Witty J F, Sheehy J E and Muller M 1983 A major error in the acetylene reduction assay: Decreases in nodular nitrogenase activity under assay conditions. J. Exp. Bot. 34, 641–649.Google Scholar
  24. Munévar F and WollumII A G 1981a Growth of Rhizobium japonicum strains at temperatures above 27°C. Appl. Environm. Microb. 42, 272–276.Google Scholar
  25. Munévar F and WollumII A G 1981b Effect of high root temperature and Rhizobium strain on nodulation, nitrogen fixation and growth of soybeans. Soil Sci. Soc. Am. J. 45, 1113–1120.CrossRefGoogle Scholar
  26. Oliveira L C Bde, Franco A A and Döbereiner J 1983 Estabilidade da efetividade e eficiência de estirpes de Rhizobium phaseoli submetidas a altas temperaturas. An. Cong. Bras. Ci. Solo, 19. Curitiba, SBCS, p. 3.Google Scholar
  27. Pankhurst C E and Gibson A H 1973 Rhizobium strain influence on disruption of clover nodule development at high root temperature. J. Gen. Microb. 74, 219–231.Google Scholar
  28. Pankhurst C E and Sprent J I 1976 Effects of temperature and oxygen tension on the nitrogenase and respiratory activities of turgid and water-stressed soybeans and French bean root nodules. J. Exp. Bot. 27, 1–9.Google Scholar
  29. Piha M I and Munns D N 1987 Sensitivity of the common bean (Phaseolus vulgaris) symbiosis to high soil temperature Plant and Soil 98, 183–194.CrossRefGoogle Scholar
  30. Rainbird R M, Atkins C A and Pate J S 1983 Effect of temperature on nitrogenase functioning in cowpea nodules. Plant Physiol. 73, 392–394.PubMedCrossRefGoogle Scholar
  31. Schubert K R and Evans H J 1976 Hydrogen evolution: A major factor affecting the efficiency of nitrogen fixation in nodulated symbionts. Proc. Natl. Acad. Sci. USA 73, 1207–1211.PubMedCrossRefGoogle Scholar
  32. Soberón-Chaves G, Nájera R, Oliveira H and Segovia L 1986 Genetic rearrangements of a Rhizobium phaseoli symbiotic plasmid. J. Bacteriol. 167, 487–491.Google Scholar
  33. Sutton W D 1983 Nodule development and senescence. In Nitrogen Fixation. Vol. 3. Ed. W JBroughton, pp 144–212. Clarendon Press, Oxford.Google Scholar
  34. Vincent J M 1970 Manual for the Practical Study of Root Nodule Bacteria. IBP Handbook nr. 15. Blackwell, Oxford. 164 p.Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • Mariangela Hungria
    • 1
    • 2
  • Avílio Antônio Franco
    • 1
    • 2
  1. 1.EMBRAPA-CNPSoLondrinaBrazil
  2. 2.EMBRAPA-CNPBSSeropédicaBrazil

Personalised recommendations