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Nodulation and nitrogen fixation in extreme environments

Abstract

Biological nitrogen fixation is a phenomenon occurring in all known ecosystems. Symbiotic nitrogen fixation is dependent on the host plant genotype, theRhizobium strain, and the interaction of these symbionts with the pedoclimatic factors and the environmental conditions. Extremes of pH affect nodulation by reducing the colonization of soil and the legume rhizosphere by rhizobia. Highly acidic soils (pH<4.0) frequently have low levels of phosphorus, calcium, and molybdenum and high concentrations of aluminium and manganese which are often toxic for both partners; nodulation is more affected than host-plant growth and nitrogen fixation. Highly alkaline soils (pH>8.0) tend to be high in sodium chloride, bicarbonate, and borate, and are often associated with high salinity which reduce nitrogen fixation. Nodulation and N-fixation are observed under a wide range of temperatures with optima between 20–30°C. Elevated temperatures may delay nodule initiation and development, and interfere with nodule structure and functioning in temperate Iegumes, whereas in tropical legumes nitrogen fixation efficiency is mainly affected. Furthermore, temperature changes affect the competitive ability ofRhizobium strains. Low temperatures reduce nodule formation and nitrogen fixation in temperate legumes; however, in the extreme environment of the high arctic, native legumes can nodulate and fix nitrogen at rates comparable to those observed with legumes in temperate climates, indicating that both the plants and their rhizobia have successfully adapted to arctic conditions. In addition to low temperatures, arctic legumes are exposed to a short growing season, a long photoperiod, low precipitation and low soil nitrogen levels. In this review, we present results on a number of structural and physiological characteristics which allow arctic legumes to function in extreme environments.

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References

  1. Alexander M 1985 Ecological constraints on nitrogen fixation in agricultural ecosystems. Adv. Microbiol. Ecol. 8, 163–183.

  2. Bell L C and Edwards D G 1987 The role of aluminium in acid soil infertility. International Board for Soil Research and Management Inc. (IBSRAM), Soil Management under Humid Conditions in Asia (ASIALAND), Proceedings of the First Regional Seminar on Soil Management under Humid Conditions in Asia and the Pacific, Khon Kaen, Phitsanulok, Thailand, October 13–20, 1986, pp 201–223.

  3. Bordeleau L M, Antoun H and Lachance R A 1977 Effects des souches deRhizobium meliloti et des coupes successives de la luzerne (Medicago sativa) sur la fixation symbiotique d'azote. Can. J. Plant Sci. 57, 433–439.

  4. Botsford J L and Lewis T A 1990 Osmoregulation inRhizobium meliloti: Production of glutamic acid in response to osmotic stress. Appl. Environ. Microbiol. 56, 488–494.

  5. Brockwell J, Pilka A and Holliday R A 1991 Soil pH is a major determinant of the numbers of naturally-occurringRhizobium meliloti in non-cultivated soils of New South Wales. Aust. J. Exp. Agric. 31, 211–219.

  6. Cloutier J, Prévost D, Nadeau P and Antoun H 1992 Heat and cold shock protein synthesis in arctic and temperate strains of rhizobia. Appl. Environ. Microbiol. 58, 2846–2853.

  7. Cralle H T and Heichel G H 1982 Temperature and chilling sensitivity of nodule nitrogenase activity of unhardened alfalfa. Crop Sci. 21, 300–304.

  8. Dawes E A 1985 Starvation, survival and energy reserves.In Bacteria in their natural environments, pp 43–79. Eds. M Fletcher and G D Floodgate, Special Publications of the Society for General Microbiology, Academic Press Inc (London).

  9. Diaz Del Castillo L 1987 Catabolisme du glucose chez desRhizobium de l'Arctique. M.Sc Thesis 8022, 60 p. Graduate School of Laval University, Québec, Canada.

  10. Diatloff A 1970 Relationship of soil moisture, temperature and alkalinity to a soybean nodulation failure. Q. J. Agric. Anim. Sci. 27, 279–293.

  11. Durand J L, Sheehy J E and Minchin F R 1987 Nitrogenase activity, photosynthesis and nodule water potential in soyabean plants experiencing water deprivation. J. Exp. Bot. 38, 311–321.

  12. Eaglesham A R J and Ayanaba A 1984 Tropical stress ecology of rhizobia, root nodulation and legume fixation.In Current Developments in Biological Nitrogen Fixation. Ed. N S Subba Rao. pp 1–35. Edward Arnold Ltd London, UK.

  13. Ek-Jander J and Fahraëus G 1971 Adaptation of rhizobia to subarctic environment in Scandinavia. Plant and Soil, Spec. Vol., 129–137.

  14. Foy C D and Lee R H 1987 Differential aluminium tolerance of two barley cultures related to organic acids in their roots. J. Plant Nutr. 10, 1089–1101.

  15. Fyson A and Sprent J I 1982 The development of primary root nodules onVicia faba L. grown at two temperatures. Ann. Bot. 50, 681–692.

  16. Gardner W K, Barber D A and Parbery D G 1983 The acquisition of phosphorus byLupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant and Soil 70, 107–124.

  17. Graham P H 1979 Influence of temperature on growth and nitrogen fixation in cultivars ofPhaseolus vulgaris L., inoculated withRhizobium. J. Agric. Sci. 93, 365–370.

  18. Graham P H 1992 Stress tolerance inRhizobium andBradyrhizobium, and nodulation under adverse soil conditions. Can. J. Microbiol. 38, 475–484.

  19. Guerin V, Trinchant J C and Rigaud J 1990 Nitrogen fixation (C2H2 reduction) by bread bean (Vicia faba L.) nodules and bacteroids under water-restricted conditions. Plant Physiol 92, 595–601.

  20. Halliday J and Pate J S 1976 The acetylene reduction assay as a means of studying nitrogen fixation in white clover under sward and laboratory conditions. J. British Grassl. Soc. 31, 29–35.

  21. Hayward H E and Wadleigh C H 1949 Plant growth on saline and alkali soils. Adv. Agron. 1, 1–38.

  22. Hong Z Q and Copeland L 1990 Pentose phosphate pathway enzymes in nitrogen-fixing leguminous root nodules. Phytochemistry 29, 2437–2440.

  23. Howieson J G, Ewing M A and D'Antuono M F 1988 Selection for acid tolerance inRhizobium meliloti. Plant and Soil 105, 179–188.

  24. Innis W E and Ingraham J E 1978 Microbial life at low temperatures: mechanisms and molecular aspects.In Microbial Life in Extreme Environments. pp 73–99. Ed D J Kushner. Academic Press, New York, NY.

  25. Karagatzides J D, Lewis M C and Schulman H M 1985 Nitrogen fixation in the high arctic tundra at Sarcpa Lake, Northwest Territories. Can. J. Bot. 63, 974–979.

  26. Karl D M 1980 Cellular nucleotide measurements and applications in microbial ecology. Microbial Rev 44, 739–796.

  27. Keyser H H and Munns D N 1979 Effects of calcium, manganese, and aluminium on growth of rhizobia in acid media. Soil Sci. Soc. Am. J. 43, 500–503.

  28. Kramer D 1984 Cytological aspects of salt tolerance in higher plants.In Salinity tolerance in plants: Strategies for crop improvements. Ed. R C Staples. John Wiley, New York, pp 3–15.

  29. Kumarasinghe R M K and Nutman P S 1979 The influence of temperature on root hair infection ofTrifolium parvfiorum andT. glomeratum by root nodule bacteria. II. The effects of changes in root temperature. J. Exp. Bot. 30, 517–528.

  30. Lakshmi-Kumari M, Singh C S and Subba Rao N S 1974 Root hair infection and nodulation in lucerne (Medicago sativa L.) as influenced by salinity and alkalinity. Plant and Soil 40, 261–268.

  31. Layzell D B, Rochman P and Canvin D T 1983 Low root temperatures and nitrogenase activity in soybean. Can. J. Bot. 62, 965–971.

  32. Lie T A 1981 Environmental physiology of the legume-Rhizobium symbiosis.In Nitrogen Fixation Vol. 1: Ecology, pp 104–134. Ed W J Broughton. Clarendon Press, Oxford.

  33. Loi A, Howieson J G, Cocks P S and Caredda S 1993 The adaptation ofMedicago polymorpha to a range of edaphic and environmental conditions-Effect of temperature on growth, and acidity stress on nodulation and nod gene induction. Aust. J. Exp. Agric. 33, 25–30.

  34. McNulty A K and Cummins W R 1987 The relationship between respiration and temperature in leaves of the arctic plantSaxifraga cernua. Plant, Cell Environ. 10, 319–325.

  35. Munns D N 1986 Acid soil tolerance in legumes and rhizobia. Adv. Plant Nutr. 2, 63–91.

  36. Munns D N and Keyser H H 1981 Tolerance of rhizobia to acidity, aluminium and phosphate. Soil Sci. Soc. Am. J. 34, 519–523.

  37. Nelson L M and Parkinson D 1978 Growth characteristics of three bacterial isolates from an arctic soil. Can. J. Microbiol. 24, 909–914.

  38. Newcomb W and Wood S W 1986 Fine structure of nitrogen-fixing leguminous root nodules from the Canadian arctic. Nordic J. Bot. 6, 609–626.

  39. Pankurst C E and Layzell D B 1984 The effect of bacterial strain and temperature changes on the nitrogenase activity ofLotus pedunculatus root nodules. Physiol. Plant. 62, 404–409.

  40. Pate J S 1977 Functional biology of dinitrogen Fixation by legumes.In A Treatise on Dinitrogen Fixation. Section III. Biology, pp 473–517. Eds R W F Hardy and W S Silver. John Wiley, Toronto.

  41. Prévost D and Bromfield E S P 1991 Effect of low root temperature on symbiotic nitrogen fixation and on competitive nodulation ofOnobrvchis viciifolia (sainfoin) by strains of arctic and temperate rhizobia. Biol. Fertil. Soils 12, 161–164.

  42. Prévost D, Antoun H and Bordeleau L M 1987a Effects of low temperatures on nitrogenase activity in sainfoin (Onobrychis viciifolia) nodulated by arctic rhizobia. FEMS (Fed.Eur. Microbiol.Soc.) Microbiol. Ecol. 45, 205–210.

  43. Prévost D, Bordeleau L M and Antoun H 1987b Symbiotic effectiveness of arctic rhizobia on a temperate forage legume sainfoin (Onobrychis viciifolia). Plant and Soil 104, 63–69.

  44. Prévost D, Bordeleau L M and Antoun H 1988 Effet des souches arctiques de Rhizobium sur la structure des nodules du Sainfoin (Onobrychis viciifolia) et de légumineuses arctiques (Astragalus etOxytropis spp.). Can. J. Bot. 67, 3164–3168.

  45. Prévost D, Bordeleau L M, Caudry-Reznick S, Schulman H M and Antoun H 1987c Characteristics of rhizobia isolated from three legume indigenous to the Canadian high arcticAstragalus alpinus, Oxytropis maydelliana andOxytropis arctobia. Plant and Soil 98, 313–324.

  46. Prévost D, Bordeleau L M, Michaud R, Lafreniére C, Waddington J and Biederbeck V O 1994 Nitrogen fixation efficiency of cold-adapted rhizobia dn sainfoin (Onobrychis viciifolia): in laboratory and field. Plant and Soil pages.

  47. Rai R 1992 Effect of acidity factors on aspects of symbiotic N2 fixation ofLens culinaris in acid soils. J. Gen. Appl. Microbiol. 38, 391–406.

  48. Rice W A 1975 Effects of CaCO3 and inoculum level on nodulation and growth of alfalfa in an acid soil. Can. J. Soil Sci. 55, 245–250.

  49. Rice W A 1982 Performance ofRhizobium meliloti strains selected for low pH tolerance. Can. J. Plant Sci. 62, 941–948.

  50. Rice W A and Olsen P E 1983 Inoculation of alfalfa seed for increased yield on moderately acid soil. Can. J. Soil Sci. 63, 541–545.

  51. Rice W A and Olsen P E 1988 Soil inoculants for alfalfa grown on moderately acid soil. Communi. in Soil Sci. Plant Anal. 19, 947–956.

  52. Rice W A, Penney D C and Nyborg M 1977 Effects of soil acidity on rhizobia numbers, nodulation and nitrogen fixation by alfalfa and red clover. Can. J. Soil Sci. 57, 197–203.

  53. Rice W A, Olsen P E and Collins M M 1992 Nitrogen fixation by alfalfa at low root temperature. First Circumpolar Agricultural Conference, Whitehorse, YT. Sept 28–Oct 2, 1992.

  54. Rieger S 1983 The genesis and classification of cold soils. Academic Press, New York, 230 p.

  55. Robson A D and Bottomley P J 1991 Limitations in the use of legumes in agriculture and forestry.In Biology and Biochemistry of Nitrogen Fixation. Ed M J Dilworth and A R Glenn, pp 320–349. Elsevier Publisher, Amsterdam, New York, Oxford, Tokyo.

  56. Schulman H M, Lewis M C, Tipping E M and Bordeleau L M 1988 Nitrogen fixation by three species ofleguminosae in the Canadian High Arctic Tundra. Plant, Cell Environ. 11, 721–728.

  57. Shannon M C 1984 Breeding, selection and the genetics of salt.In Salinity tolerance in plants: Strategies for crop improvement. Ed. R C Staples. John Wiley, New York, pp 231–254.

  58. Sprent J I 1984 Effects of drought and salinity on heterotrophic nitrogen fixing bacteria and on infection of legumes by rhizobia.In Advances in Nitrogen Fixation Research, pp 295–302. Ed C Veeger and W E Newton. Martinus Nijhoff, The Hague.

  59. Sprent J I and Zahran H H 1988 Infection, development and functioning of nodules under drought and salinity.In Nitrogen fixation by legumes in Mediterranean agriculture, pp 145–151. Eds D P Beck and L A Materon. Martinus Nijhoff/Dr. W. Junk, Dordrecht.

  60. Tang C and Robson A 1993 pH above 6.0 reduces nodulation inLupinus species. Plant and Soil 152, 269–276.

  61. Taylor R W, Sistani K R and Patel S 1990 Soybean-Rhizobium combination for tolerance to low P-high aluminium. J. Agron. Crop Sci 165, 54–60.

  62. Tieszen L L, Lewis M C, Miller P C, Mayo J, Chapin F S and Oechel W 1981 An analysis of primary production in tundra growth forms.In Tundra ecosystems: a comparative analysis, pp 285–386. Eds L C Bliss, O W Heal and J J Moore, Cambridge University Press, Cambridge.

  63. Tipping E M 1984 Symbiotic dinitrogen fixation inOxytropis maydelliana Trautv., an arctic legume. M.Sc Thesis 6105, 92 p. Graduate School Laval University, Quebec, Canada.

  64. Trinick M J 1982 Biology.In Nitrogen Fixation, Vol. 2:Rhizobium, pp 76–146. Ed W J Broughton. Clarence Press, Oxford.

  65. Vargas A A T and Graham P H 1988Phaseolus vulgaris cultivar andRhizobium strain variation in acid-pH tolerance and nodulation under acid conditions. Field Crops Res. 19, 91–101.

  66. Waughman G J 1977 The effect of temperature on nitrogenase activity. J. Exp. Bot. 28, 949–960.

  67. Yadav N K and Vyas S R 1971 Response of root-nodule rhizobia to saline, alkaline and acid conditions. Indian J. Agric. Sci. 41, 875–881.

  68. Zahran H H 1991 Conditions for successfulRhizobium-legume symbiosis in saline environments. Biol. Fertil. Soils 12, 73–80.

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Bordeleau, L.M., Prévost, D. Nodulation and nitrogen fixation in extreme environments. Plant Soil 161, 115–125 (1994). https://doi.org/10.1007/BF02183092

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Key words

  • nodulation
  • nitrogenase
  • adaptation
  • extreme environments
  • arctic rhizobia