Advertisement

Biology and Fertility of Soils

, Volume 46, Issue 8, pp 861–875 | Cite as

Effect of two species of cyanobacteria as biofertilizers on some metabolic activities, growth, and yield of pea plant

  • Mohamed Elanwar H. OsmanEmail author
  • Mostafa M. El-Sheekh
  • Amal H. El-Naggar
  • Saly F. Gheda
Original Paper

Abstract

Two cyanobacterial species (Nostoc entophytum and Oscillatoria angustissima) were tested as biofertilizers, substituting the normally used chemical fertilizer, for pea plant. Inoculation of soil with a suspension of each species or a combination of the two species significantly increased the germination percentage and stimulated the other measured growth parameters and photosynthetic pigment fractions of pea. However, the soil inoculation with one cyanobacterial species and the addition of the recommended dose or half the recommended dose of chemical fertilizer were usually more effective and also increased carbohydrate and protein contents of produced pea seeds. However, biofertilization combined with half the recommended dose of the chemical fertilizer was usually more effective than the addition of the full rate of the chemical fertilizer, and this may allow saving 50% of the used chemical fertilizer. The protein profile of the produced seeds showed appearance and disappearance of some protein bands in response to fertilization treatments compared to the control. Blue green algae analyses show that N. entophytum fixed more N, produced more exopolysaccharide, and contained more auxin and cytokinin than O. angustissima, the latter contained more gibberellins. These data may explain their different influences on growth and yield of pea.

Keywords

Cyanobacteria Biofertilizers Plant growth Pea Phytohormones 

Notes

Acknowledgment

The authors are grateful to Editor-in-Chief Prof. Paolo Nannipieri and two anonymous reviewers for valuable comments and criticism which significantly improved this manuscript.

References

  1. Abd-Allah MH, Mahmoud ALE, Issa AA (1994) Cyanobacterial biofertilizers improved growth of wheat. Phyton 34:11–18, HornGoogle Scholar
  2. Adam MS (1999) The promotive effect of the cyanobacterium Nostoc muscorum on the growth of some crop plants. Acta Microbiol Pol 48:163–171Google Scholar
  3. Allen MM, Stanier ST (1968) Selective isolation of blue green algae from water and soil. J Gen Microbiol 51:203PubMedGoogle Scholar
  4. Allen SE, Grinshaw HM, Parkinson JA, Quarmby C (1974) Chemical analysis of ecological materials. Blackwell Scientific Publications, Oxford, p 565Google Scholar
  5. Asari N, Ishihara R, Nakajima Y, Kimura M, Asakawa S (2008) Cyanobacterial communities of rice straw left on the soil surface of a paddy field. Biol Fertil Soils 44:605–612CrossRefGoogle Scholar
  6. Bobade KP, Kolte SO, Patil BG (1992) Affectivity of cyanobacterial technology for transplanted rice. Phykos 31:33–35Google Scholar
  7. Bograh A, Gingras Y, Tajmir R, Carpentier R (1997) The effects of spermine and spermidine on the structure of photosystem II proteins in relation to inhibition of electron transport. FEBS Lett 402:41–44CrossRefPubMedGoogle Scholar
  8. Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilization the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  9. Carmichael WW (1994) The toxins of cyanobacteria. Sci Am 270:64–72CrossRefGoogle Scholar
  10. Choudhury S, Gupta K (1998) Studies on the germination mechanism of Catharanthus roseus (L.) G. Do NCV. Alba seeds effect of promoters and pH-Seed. Sci Technol 26:719–732Google Scholar
  11. Choudhury ATMA, Kennedy IR (2004) Prospects and potentials for systems of biological nitrogen fixation in sustainable rice production. Biol Fertil Soils 39:219–227CrossRefGoogle Scholar
  12. Davies PJ (1995) Plant hormones. Kluwer Academic Publishers, Dordrecht, The Netherlands, p 192Google Scholar
  13. De Caire GZ, De Cano MS, De Mule MCZ, Palma RM, Colombo K (1997) Exopolysaccharide of Nostoc muscorum (cyanobacteria) in the aggregation of soil particles. J Appl Phycol 9:249–253CrossRefGoogle Scholar
  14. De Caire GZ, De Cano MS, Palma RM, De Mule MCZ (2000) Changes in soil enzyme activities following additions of cyanobacterial biomass and exopolysaccharide. Soil Biol Biochem 32:1985–1987CrossRefGoogle Scholar
  15. De Cano MS, De Mule MCZ, De Caire GZ, De Halperin DR (1993) Biofertilization of rice plants with the cyanobacterium Tolypothrix tenuis (40d). Phyton B Aires 54:149–155Google Scholar
  16. De Cano SM, De Mule ZMC, De Caire ZG, Palma RM, Colombo K (1997) Aggregation of soil particles by Nostoc muscorum (Cyanobacteria). Int J Exp Bot 57:35–40, phytonGoogle Scholar
  17. De Cano MMS, De Caire GZ, De Mulé MCZ, Palma RM (2002) Effect of Tolypothrix tenuis and Microchaete tenera on biochemical soil properties and maize growth. J Plant Nutr 25:2421–2431CrossRefGoogle Scholar
  18. Drazkiewicz M (1994) Chlorophyllase: occurrence, functions, mechanism of action, effect of external and internal factors. Phytosynthetica 30:321–331Google Scholar
  19. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric methods for determination of sugars and related substances. Am Chem Soc 23:351–359Google Scholar
  20. Featonby-Smith BC, Van Staden J (1983) The effect of seaweed concentrate and fertilizer on the growth of Beta vulgaris. Zpflanzenphysiol 112:155–162Google Scholar
  21. Halder AK, Mishra AK, Chakrabarty PK (1991) Solubilization of inorganic phosphates by Bradyrhizobium. Indian J Exp Biol 29:28–31Google Scholar
  22. Hardy RWF, Burns RC, Holsten RD (1973) Applications of the acetylene-ethylene assay for measurement of nitrogen fixation. Soil Biol Biochem 5:47–48CrossRefGoogle Scholar
  23. Haroun SA, Hussein MH (2003) The promotive effect of algal biofertilizers on growth, protein pattern and some metabolic activities of Lupinus termis plants grown in siliceous soil. Asian J Plant Sci 2:944–951CrossRefGoogle Scholar
  24. Jha MN, Prasad AN (2006) Efficacy of new inexpensive cyanobacterial biofertilizer including its shelf-life. World J Microbiol Biotechnol 22:73–79CrossRefGoogle Scholar
  25. Jones HG, Davies WJ (1991) A perspective on ABA research in the 1990s. In: Davies WJ, Jones HG (eds) Abscisic acid, physiology and biochemistry. Bios. Scientific Publishers, Oxford, pp 1–4Google Scholar
  26. Karthikeyan N, Prasanna R, Nain L, Kaushik BD (2007) Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. Euro J Soil Biol 43:23–30CrossRefGoogle Scholar
  27. King J (1991) The genetic basis of plant physiological processes. Oxford University Press, Oxford, p 413Google Scholar
  28. Kowolczyck M, Sandberg G (2001) Quantitative analysis of indole-3-acetic acid metabolites in Arabidopsis. Plant Physiol 127:1845–1853CrossRefGoogle Scholar
  29. Kulhlbusch TA, Lobert JM, Crutzen PJ, Warneck P (1991) Molecular nitrogen emission. Trace nitrification during biomass burning. Nature 351:135–137CrossRefGoogle Scholar
  30. Kumar V, Basra AS, Malik CB (1987) Enzymes of nonphotosynthetic C4-dicarboxylic acid metabolism in germinating grains of wheat. Biochem Physiol Pflazen 182:261–262Google Scholar
  31. Laemmili UK (1970) Cleavage of structural proteins during the assembly of the head of Bacteriophage T4. Nature 227:680–685CrossRefGoogle Scholar
  32. Lee YP, Takahashi T (1966) An improved colorimeteric determination of amino acids with the use of nin hydrin. Anal Biochem 14:71–75CrossRefGoogle Scholar
  33. Likhitkar VS, Tarar JL (1995) Effect of presoaking seed treatment with Nostoc muscorum extracts on cotton. Ann Plant Physiol 9:113–116Google Scholar
  34. Lozano MS, Verde Star J, Maiti RK, Oranday CA, Gaona RH, Aranda HE, Rojas GM (1999) Effect of an algal extract and several plant growth regulators on the nutritive value of potatoes (Solanum tuberosum L. var. gigant). Arch Latinoam Nutr 49:166–170Google Scholar
  35. Malam Issa O, Défarge C, Le Bissonnais Y, Marin B, Duval O, Bruand A, D'Acqui LP, Nordenberg S, Annerman M (2007) Effects of the inoculation of cyanobacteria on the microstructure and the structural stability of a tropical soil. Plant Soil 290:209–219CrossRefGoogle Scholar
  36. Maqubela MP, Mnkeni PNS, Malam Issa O, Pardo MT, D'Acqui LP (2009) Nostoc cyanobacterial inoculation in South African agricultural soils enhances soil structure, fertility and maize growth. Plant Soil 315:79–92CrossRefGoogle Scholar
  37. McElhiney J, Lawton LA, Leifert C (2001) Investigations into the inhibitory effects of microcystins on plant growth and the toxicity of plant tissues following exposure. Toxicon 39:1411–1420CrossRefPubMedGoogle Scholar
  38. Mckinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322Google Scholar
  39. Metzner H, Rau H, Senger H (1965) Untersuchunger, zur synchronisierbarkei einzelner pigmentmangel mutanten von Chlorella. Planta 65:186–194CrossRefGoogle Scholar
  40. Mishra U, Pabbi S (2004) Cyanobacteria: a potential biofertilizer for rice. Resonance 9:6–10CrossRefGoogle Scholar
  41. Mohiuddin M, Das AK, Ghosh DC (2000) Growth and productivity of wheat as influenced by integrated use of chemical fertilizer, biofertilizer and growth regulator. Indian J Plant Physiol 5:334–338Google Scholar
  42. Nelson N (1944) Aphotometric adaptation of somagi method for the determination of glucose. J Biol Chem 153:275Google Scholar
  43. Nilsson M, Bhattacharya J, Rai AN, Bergman B (2002) Colonization of roots of rice (Oryza sativa) by symbiotic Nostoc strains. New Phytol 156:517–525CrossRefGoogle Scholar
  44. Nisha R, Kaushik A, Kaushik CP (2007) Effect of cyanobacterial application on structural stability and productivity of an organically poor semi-arid soil. Geoderma 138:49–56CrossRefGoogle Scholar
  45. Obana S, Miyamoto K, Morita S, Ohmori M, Inubushi K (2007) Effect of Nostoc sp. On soil characteristics, plant growth and nutrient up take. J Appl Phycol 19:641–646CrossRefGoogle Scholar
  46. Obreht Z, Nw K, Gantar M, Rowell P (1993) Effects of root associated N2-fixing cyanobacteria on the growth and nitrogen content of wheat (Triticum vulgare L.) seedlings. Biol Fertil Soils 15:68–72CrossRefGoogle Scholar
  47. Okalo BN, Ezeogu LI, Ebisike CO (1996) Raw starch digesting amylase from Thermoactinomyces thalophilus F13. World J Microbiol Biotechnol 12:637–638CrossRefGoogle Scholar
  48. Ördög V (1999) Beneficial effects of microalgae and cyanobacteria in plant/soil system with special regard to their auxin and cytokinin-like activity. International workshop and training course on microalgal biology and biotechnology, Mosonmagyaróvár, Hungary, June 13–26, UNESCO (International Cell Research Organization), pp 43–44Google Scholar
  49. Pandey KD, Shukla PN, Giri DD, Kashyap AK (2005) Cyanobacteria in alkaline soil and the effect of cyanobacteria inoculation with pyrite amendments on their reclamation. Biol Fertil Soils 41:451–457CrossRefGoogle Scholar
  50. Pereira I, Ortega R, Barrientos L, Moya M, Reyes G, Kramm V (2009) Development of a biofertilizer based on filamentous nitrogen-fixing cyanobacteria for rice crops in Chile. J Appl Phycol 21:135–144CrossRefGoogle Scholar
  51. Periminova GN (1972) Methods of study and practical use of soil algae. Report Kirov & Agric Inst Kirov, p 221 (In Russian)Google Scholar
  52. Popova LP, Stoinova ZG, Maslenkova LT (1995) Involvement of abscisic acid in photosynthetic process in Hordeum vulgare L. during salinity stress. J Plant Growth Regul 14:211–218CrossRefGoogle Scholar
  53. Prasad BK, Kumar M, Kumar R, Kumar SK, Kumar V, Diwakar AP, Singh KR, Prasad U (2000) Effect of domestic wastes on the germination of maize and cowpea seeds. J Phytol Res 13:191–194Google Scholar
  54. Prescott GW (1962) Algae of western great lakes area. Wm. C. Brown, Dubuque, IAGoogle Scholar
  55. Prescott GW (1970) How to know the fresh water algae. Wm. C. Brown, Dubuque, IAGoogle Scholar
  56. Roger PA, Santiago-Ardales S, Watanabe I (1986) Nitrogen fixing blue-green algae in rice soils of northern Luzon (Philippines). Phil Agr 69:589–598Google Scholar
  57. Rogers SL, Burns RG (1994) Changes in aggregate stability, nutrient status, indigenous microbial populations and seedlings emergence following inoculation of soil with Nostoc muscorum. Biol Fertil Soils 18:209–215CrossRefGoogle Scholar
  58. Saadatnia H, Riahi H (2009) Cyanobacteria from paddy fields in Iran as a biofertilizer in rice plants. Plant Soil Environ 55:207–212Google Scholar
  59. Sapatnekar HG, Rasal PH, Patil PL (2001) Effects of N2-fixers along with inorganic fertilizers on paddy yield. J Maharashtra Agr Univ 26:118–119Google Scholar
  60. Saswati-Nayak R-P, Pabby A, Dominic TK, Singh PK (2004) Effect of urea, blue green algae and Azolla on nitrogen fixation and chlorophyll accumulation in soil under rice. Biol Fertil Soils 40:67–72CrossRefGoogle Scholar
  61. Serdyuk OP, Smolygina LP, Kobzar EV, Gogotov IN (1992) Phytohormones formed by the nitrogen fixing association of Anabaena–Azollae. Doklady Biochem 325:149–151Google Scholar
  62. Sinha RP, Kumar A (1992) Screening of blue-green algae for biofertilizer. In: Patil, P. S (ed) Proceedings of the national seminar on organic farming, Pune, India, pp 95–97Google Scholar
  63. Sinha SK, Verma DC, Dwivedi CP (2002) Role of green manure (Sesbania rostrata) and biofertilizers (Blue-green algae and Azotobactor) in rice-wheat cropping system in state of Uttar Pradesh, India. Physiol Mol Biol Plants 8:105–110Google Scholar
  64. SPSS (2006) SPSS base user's guide 15.0. SPSS, Chicago, p 618Google Scholar
  65. Stirk WA, Ördög V, Van Staden J (1999) Identification of cytokinin isopentenyladenine in a strain of Arthronema africanum (cyanobacteria). J Phycol 35:89–92CrossRefGoogle Scholar
  66. Stirk WA, Ördög V, Van Staden J, Jäger K (2002) Cytokinin and auxin like activity in cyanophyta and microalgae. J Appl Phycol 14:215–221CrossRefGoogle Scholar
  67. Vaishampayan A, Sinha RP, Häder DP, Dey T, Gupta AK, Bhan U, Rao AL (2001) Cyanobacterial biofertilizers in rice agriculture. Bot Rev 67:453–516CrossRefGoogle Scholar
  68. Van den Berg DJC, Robijn GW, Janssen AC, Giuseppin MLF, Vreeker R, Kamerling JP, Vliegenthart JFG, Lebeboer AM, Verrips CT (1995) Production of a novel extracellular polysaccharide by Lactobacillus Sake-01 and characterization of the polysaccharide. Appl Environ Microbiol 61:2840–2844PubMedGoogle Scholar
  69. Van Kessel C, Hartley C (2000) Agricultural management of grain legumes: has it led to an increase in nitrogen fixation? Field Crop Res 65:165–181CrossRefGoogle Scholar
  70. Venkataraman GS (1969) The cultivation of algae. Indian Council of Agricultural Research, New Delhi, p 319Google Scholar
  71. Wang SM, Wang QL, Li SH, Zhang JR (1991) A study of treatment of spring wheat with growth promoting substances from nitrogen-fixing blue green algae. Acta Hydrob Sin 15:45–52Google Scholar
  72. Waters ERI, Lea GJ, Vierling E (1996) Evaluation, structure and function of the small heat shock proteins. J Exp Bot 47:325–338CrossRefGoogle Scholar
  73. Whitton BA (2000) Soils and rice-fields. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Kluwer Academic Publishers, Dordrecht, pp 233–255Google Scholar
  74. Wiegand C, Pflugmacher S (2005) Ecotoxicological effects of selected cyanobacterial secondary metabolites: a short review. Toxicol App Pharmacol 203:201–218CrossRefGoogle Scholar
  75. Yanni YG (1991) Protection of rice against “rosette long-day” disorder by inoculation with Aulosira fertilissima vs treatment with gibberellic acid. World J Microbiol Biotechnol 7:436–438CrossRefGoogle Scholar
  76. Younis ME, El-Shahaby OA, Abo-Hamed SA, Haroun SA (1991) Plant growth, metabolism and adaptation in relation to stress conditions. XI. Modification of osmotic-stress-induced metabolic effects by GA3 or IAA in Pisum sativum plants. Acta Agron Hung 40:367–375Google Scholar
  77. Zaccaro MC, De Caire GZ, De Cano MS, Palma RM, Colombo K (1999) Effect of cyanobacterial inoculation and fertilizers on rice seedlings and postharvest soil structure. Comm Soil Sci Plant Anal 30:97–107CrossRefGoogle Scholar
  78. Zaccaro MC, Salazar C, De Caire GZ, De Cano MS, Stella AM (2001) Lead toxicity in cyanobacterial porphyrin metabolism. Environ Toxicol Water Qual 16:61–67Google Scholar
  79. Zheleva DT, Tsonev T, Sergiev I, Karanov E (1994) Protective effect of exogenous polyamines against atrazine in pea plants. J Plant Growth Regul 13:203–211CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Mohamed Elanwar H. Osman
    • 1
    Email author
  • Mostafa M. El-Sheekh
    • 1
  • Amal H. El-Naggar
    • 1
  • Saly F. Gheda
    • 1
  1. 1.Botany Department, Faculty of ScienceTanta UniversityTantaEgypt

Personalised recommendations