Advertisement

Plant and Soil

, Volume 370, Issue 1–2, pp 317–332 | Cite as

Nostoc, Microcoleus and Leptolyngbya inoculums are detrimental to the growth of wheat (Triticum aestivum L.) under salt stress

  • William S. Cuddy
  • Brett A. Summerell
  • Michelle M. Gehringer
  • Brett A. Neilan
Regular Article

Abstract

Background and aims

This study investigated the effect of cyanobacterial inoculants on salt tolerance in wheat.

Methods

Unicyanobacterial crusts of Nostoc, Leptolyngbya and Microcoleus were established in sand pots. Salt stress was targeted at 6 and 13 dS m−1, corresponding to the wheat salt tolerance and 50 % yield reduction thresholds, respectively. Germinated wheat seeds were planted and grown for 14 (0 and 6 dS m−1) and 21 (13 dS m−1) days by which time seedlings had five emergent leaves. The effects of cyanobacterial inoculation and salinity on wheat growth were quantified using chlorophyll fluorescence, inductively coupled plasma-optical emission spectrometry and biomass measurements.

Results

Chlorophyll fluorescence was negatively affected by soil salinity and no change was observed in inoculated wheat. Effective photochemical efficiency correlated with a large range of plant nutrient concentrations primarily in plant roots. Inoculation negatively affected wheat biomass and nutrient concentrations at all salinities, though the effects were fewer as salinity increased.

Conclusions

The most likely explanation of these results is the sorption of nutrients to cyanobacterial extracellular polymeric substances, making them unavailable for plant uptake. These results suggest that cyanobacterial inoculation may not be appropriate for establishing wheat in saline soils but that cyanobacteria could be very useful for stabilising soils.

Keywords

Cyanobacteria Nostoc Microcoleus Biological soil crust Wheat Salinity 

Notes

Acknowledgments

We thank Pacific Seeds and Agrigrain Limited for providing seeds of Triticum aestivum L. ‘EGA Gregory’. We thank Dr. Murray Badger and Dr. Britta Forster of the Australian National University for assistance with Pulse Amplitude Modulation Fluorometry. A scholarship for W.S.C. was provided by the Grains Research and Development Corporation, Australia. The other authors are funded by the Australian Research Council, the Australian Centre for Astrobiology and the Royal Botanic Gardens and Domain Trust, Sydney, Australia.

References

  1. Abd El-Baky HH, El-Baz FK, El Baroty GS (2008) Enhancing antioxidant availability in wheat grains from plants grown under seawater stress in response to microalgae extract treatments. J Sci Food Agric 90:299–303CrossRefGoogle Scholar
  2. Ahmed M, Stal LJ, Hasnain S (2010) Association of non-heterocystous cyanobacteria with crop plants. Plant Soil 336:363–375CrossRefGoogle Scholar
  3. Alloway BJ (2009) Soil factors associated with zinc deficiency in crops and humans. Environ Geochem Health 31:537–548PubMedCrossRefGoogle Scholar
  4. Atak M, Kaya MD, Kaya G, Çikili Y, Çiftçi CY (2006) Effects of NaCl on the germination, seedling growth and water uptake of Triticale. Turk J Agric 30:39–47Google Scholar
  5. Aziz MA, Hashem MA (2003) Role of cyanobacteria in improving fertility of saline soil. Pakistan J Biol Sci 6:1751–1752CrossRefGoogle Scholar
  6. Aziz MA, Hashem MA (2004) Role of cyanobacteria on yield of rice in saline soil. Pakistan J Biol Sci 7:309–311CrossRefGoogle Scholar
  7. Belkhodja R, Morales F, Abadia A, Medrano H, Abadia J (1999) Effects of salinity on chlorophyll fluorescence and photosynthesis of barley (Hordeum vulgare L.) grown under triple-line-source sprinkler system in the field. Photosynth 36:375–387CrossRefGoogle Scholar
  8. Belnap J, Gillette DA (1998) Vulnerability of desert biological soil crusts to wind erosion: the influences of crust development, soil texture, and disturbance. J Arid Environ 39:133–142CrossRefGoogle Scholar
  9. Benavides MP, Marconi PL, Gallego SM, Comba ME, Tomaro ML (2000) Relationship between antioxidant defense systems and salt tolerance in Solanum tuberosum. Funct Plant Biol 27:273–278CrossRefGoogle Scholar
  10. Bhaskar PV, Bhosle NB (2006) Bacterial extracellular polymeric substance (EPS): a carrier of heavy metals in the marine food-chain. Environ Internat 32:191–198CrossRefGoogle Scholar
  11. Blanco A, Sanz B, Llama MJ, Serra JL (1998) Reutilization of non-viable biomass of Phormidium laminosum for metal biosorption. Biotechnol Appl Biochem 27:167–174Google Scholar
  12. Blanco A, Sanz B, Llama MJ, Serra JL (1999) Biosorption of heavy metals to immobilised Phormidium laminosum biomass. J Biotechnol 69:227–240CrossRefGoogle Scholar
  13. Charman PEV, Wooldridge AC (2000) Soil chemical properties: Soil salinisation. In: Charman PEV, Murphy BW (eds) Soils: their properties and management. Oxford University Press, Melbourne, Oxford, pp 237–245Google Scholar
  14. de Philippis R, Paperi R, Sili C, Vincenzini M (2003) Assessment of the metal removal capability of two capsulated cyanobacteria, Cyanospira capsulata and Nostoc PCC7936. J Appl Phycol 15:155–161CrossRefGoogle Scholar
  15. de Philippis R, Paperi R, Sili C (2007) Heavy metal sorption by released polysaccharides and whole cultures of two exopolysaccharide-producing cyanobacteria. Biodegrad 18:181–187CrossRefGoogle Scholar
  16. Decho AW (2000) Microbial biofilms in intertidal systems: an overview. Cont Shelf Res 20:1257–1273CrossRefGoogle Scholar
  17. R Development Core Team (2010) R: a language and environment for statistical computing. 2.12.0 edn. R Foundation for statistical computing, Vienna, AustriaGoogle Scholar
  18. El-Hendawy SE, Hu Y, Schmidhalter U (2005a) Growth, ion content, gas exchange, and water relations of wheat genotypes differing in salt tolerances. Aust J Agric Res 56:123–134CrossRefGoogle Scholar
  19. El-Hendawy SE, Hu Y, Yakout GM, Awad AM, Hafiz SE, Schmidhalter U (2005b) Evaluating salt tolerance of wheat genotypes using multiple parameters. Eur J Agron 22:243–253CrossRefGoogle Scholar
  20. Flemming H-C (2011) The perfect slime. Colloid Surface B 86:251–259CrossRefGoogle Scholar
  21. Gantar M (2000) Mechanical damage of roots provides enhanced colonisation of the wheat endorhizosphere by dinitrogen-fixing cyanobacterium Nostoc sp. strain 2S9B. Biol Fert Soils 32:250–255CrossRefGoogle Scholar
  22. Gantar M, Elhai J (1999) Colonization of wheat para-nodules by the N2-fixing cyanobacterium Nostoc sp. strain 2S9B. New Phytol 141:373–379CrossRefGoogle Scholar
  23. Gantar M, Kerby NW, Rowell P (1991a) Colonisation of wheat (Triticum vulgare L.) by N2-fixing cyanobacteria: II. An ultrastructural study. New Phytol 118:485–492CrossRefGoogle Scholar
  24. Gantar M, Kerby NW, Rowell P, Obreht Z (1991b) Colonisation of wheat (Triticum vulgare L.) by N2-fixing cyanobacteria: I. A survey of soil cyanobacterial isolates forming associations with roots. New Phytol 118:477–483CrossRefGoogle Scholar
  25. Gantar M, Kerby NW, Rowell P (1993) Colonisation of wheat (Triticum vulgare L.) by N2-fixing cyanobacteria: III. The role of a hormogonia-promoting factor. New Phytol 124:505–513CrossRefGoogle Scholar
  26. Gantar M, Kerby NW, Rowell P, Obreht Z, Scrimgeour C (1995a) Colonisation of wheat (Triticum vulgare L.) by N2-fixing cyanobacteria: IV. Dark nitrogenase activity and effects of cyanobacteria on natural 15N abundance in the plants. New Phytol 129:337–343CrossRefGoogle Scholar
  27. Gantar M, Rowell P, Kerby NW, Sutherland IW (1995b) Role of extracellular polysaccharide in the colonization of wheat (Triticum vulgare L.) roots by N2-fixing cyanobacteria. Biol Fertil Soils 19:41–48CrossRefGoogle Scholar
  28. Garcia-Pichel F, Belnap J (1996) Microenvironments and microscale productivity of cyanobacterial desert crusts. J Phycol 32:774–782CrossRefGoogle Scholar
  29. Genc Y, McDonald GK, Tester M (2007) Reassessment of tissue Na+ concentration as a criterion for salinity tolerance in bread wheat. Plant Cell Env 30:1486–1498CrossRefGoogle Scholar
  30. Gorelova OA (2006) Communication of cyanobacteria. Microbiol 75:465–469CrossRefGoogle Scholar
  31. Hashem MA (2001) Problems and prospects of cyanobacterial biofertiliser for rice cultivation. Aust J Plant Physiol 28:881–888Google Scholar
  32. Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. University of California, College of Agriculture, Agricultural Experiment Station, BerkelyGoogle Scholar
  33. Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Phys Plant Mol Biol 47:655–684CrossRefGoogle Scholar
  34. Hu Y, Schmidhalter U (1997) Interactive effects of salinity and macronutrient level on wheat II. Composition. J Plant Nutr 20:1169–1182CrossRefGoogle Scholar
  35. Hu C, Liu Y, Song L, Zhang D (2002) Effect of desert soil algae on the stabilization of fine sands. J Appl Phycol 14:281–292CrossRefGoogle Scholar
  36. Hu C, Liu Y, Paulsen BS, Petersen D, Klaveness D (2003) Extracellular carbohydrate polymers from five desert soil algae with different cohesion in the stabilization of find sand grain. Carbohydr Polym 54:33–42CrossRefGoogle Scholar
  37. Husain S, von Caemmerer S, Munns R (2004) Control of salt transport from roots to shoots of wheat in saline soil. Funct Plant Biol 31:1115–1126CrossRefGoogle Scholar
  38. Islam S, Malik AI, Islam AKMR, Colmer TD (2007) Salt tolerance in a Hordeum vulgare - Triticum aestivum amphiploid, and its parents. J Exp Bot 58:1219–1229PubMedCrossRefGoogle Scholar
  39. Issa AA, Abd-Alla MH, Mahmoud A-LE (1994) Effect of biological treatments on growth and some metabolic activities of barley plants grown in saline soil. Microbiol Res 149:317–320CrossRefGoogle Scholar
  40. Karthikeyan N, Prassana R, Nain L, Kaushik BD (2007) Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. Eur J Soil Biol 43:23–30CrossRefGoogle Scholar
  41. Karthikeyan N, Prassana R, Sood A, Jaiswal P, Nayak S, Kaushik BD (2009) Physiological characterisation and electron microscopic investigation of cyanobacteria associated with wheat rhizosphere. Folia Microbiol 54:43–51CrossRefGoogle Scholar
  42. Kennedy IR, Islam N (2001) The current and potential contribution of asymbiotic nitrogen fixation to nitrogen requirements on farms: a review. Aust J Exp Agric 41:447–457CrossRefGoogle Scholar
  43. Kennedy IR, Choudhury ATMA, Kecskes ML (2004) Non-symbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better exploited? Soil Biol Biochem 36:1229–1244CrossRefGoogle Scholar
  44. Khattak RA, Jarrell WM, Page AL (1989) Mechanism of native manganese release in salt-treated soils. Soil Sci Soc Am J 53:701–705CrossRefGoogle Scholar
  45. Logan BA, Adams WWI, Demmig-Adams B (2007) Avoiding common pitfalls of chlorophyll fluorescence analysis under field conditions. Funct Plant Biol 34:853–859CrossRefGoogle Scholar
  46. Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398CrossRefGoogle Scholar
  47. Maas EV (1986) Salt tolerance of plants. Appl Agr Res 1:12–26Google Scholar
  48. Maas EV, Hoffman GJ, Asce M (1977) Crop salt tolerance- current assessment. J Irr Drain Div 103:115–134Google Scholar
  49. Mager DM, Thomas AD (2011) Extracellular polysaccharides from cyanobacterial soil crusts: a review of their role in dryland soil processes. J Arid Environ 75:91–97CrossRefGoogle Scholar
  50. Malam Issa O, Defarge 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
  51. Maqubela MP, Mnkeni PNS, Malam Issa O, Pardo MT, D’Acqui LP (2009) Nostoc cyanobacterial inoculation in South African soils enhances soil structure, fertility, and maize growth. Plant Soil 315:79–92CrossRefGoogle Scholar
  52. Mashali AM (1999) Land degradation with focus on salinization and its management in Africa. In: Nabhan H, Mashali AM, Mermut AR (eds) Integrated soil management for sustainable agriculture and food security in southern and east Africa. Food and Agriculture Organization of the United Nations, Rome, pp 17–47Google Scholar
  53. Maxwell K, Johnson GN (2000) Chorophyll fluorescence- a practical guide. J Exp Bot 51:659–668PubMedCrossRefGoogle Scholar
  54. Mazhar S, Hasnain S (2011) Screening of native plant growth promoting cyanobacteria and their impact on Triticum aestivum var. Uqab 2000 growth. Afr J Agric Res 6:3988–3993Google Scholar
  55. Mazor G, Kidron GJ, Vonshak A, Abeliovich A (1996) The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts. FEMS Microbiol Ecol 21:121–130CrossRefGoogle Scholar
  56. Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P, Atlas R (2001) An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res 70:85–106PubMedCrossRefGoogle Scholar
  57. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663PubMedCrossRefGoogle Scholar
  58. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  59. Munns R, James RA, Lauchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043PubMedCrossRefGoogle Scholar
  60. Nain L, Rana A, Joshi M, Jadhav SD, Kumar D, Shivay YS, Paul S, Prasanna R (2010) Evaluation of synergistic effects of bacterial and cyanobacterial strains as biofertilizers for wheat. Plant Soil 331:217–230CrossRefGoogle Scholar
  61. Nilsson M, Rasmussen U, Bergman B (2005) Competition among symbiotic cyanobacterial Nostoc strains forming artificial associations with rice (Oryza sativa). FEMS Microbiol Lett 245:139–144PubMedCrossRefGoogle Scholar
  62. Nilsson M, Rasmussen U, Bergman B (2006) Cyanobacterial chemotaxis to extracts of host and nonhost plants. FEMS Microbiol Ecol 55:382–390PubMedCrossRefGoogle Scholar
  63. Obreht Z, Kerby NW, 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 Fert Soils 15:68–72CrossRefGoogle Scholar
  64. Ozturk S, Aslim B (2010) Modification of exopolysaccharide composition and production by three cyanobacterial isolates under salt stress. Environ Sci Pollut Res 17:595–602CrossRefGoogle Scholar
  65. Pardo MT, Almendros G, Zancada MC, Lopez-Fando C (2010) Biofertilization of degraded South African soils with cyanobacteria affects organic matter content and quality. Arid Land Res Manag 24:328–343CrossRefGoogle Scholar
  66. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotox Environ Safe 60:324–349CrossRefGoogle Scholar
  67. Pradhan S, Rai LC (2001) Biotechnological potential of Microcystis sp. in Cu, Zn, and Cd biosorption from single and multimetallic systems. BioMetals 14:67–74PubMedCrossRefGoogle Scholar
  68. Rascio A, Russo M, Mazzucco L, Plattani C, Nicastro G, Di Fonzo N (2001) Enhanced osmotolerance of a wheat mutant selected for potassium accumulation. Plant Sci 160:441–448PubMedCrossRefGoogle Scholar
  69. Rasmussen U, Johansson C, Bergman B (1994) Symbiosis: plant-induced cell differentiation and protein synthesis in the Cyanobacterium. Mol Plant Microbe Interact 7:696–702CrossRefGoogle Scholar
  70. Rengasamy P (2002) Transient salinity and subsoil constraints to dryland farming in Australian sodic soils: an overview. Aust J Exp Agric 42:351–361CrossRefGoogle Scholar
  71. Rengasamy P (2006) World salinization with emphasis on Australia. J Exp Bot 57:1017–1023PubMedCrossRefGoogle Scholar
  72. Richards LA (1954) Diagnosis and improvement of saline and alkali soils. United States Department of Agriculture, Washington D. CGoogle Scholar
  73. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61CrossRefGoogle Scholar
  74. Rodriguez AA, Stella AM, Storni MM, Zulpa G, Zaccaro MC (2006) Effects of cyanobacterial extracellular products and gibberellic acid on salinity tolerance in Oryza sativa L. Saline Syst 2Google Scholar
  75. Sayed HI (1985) Diversity of salt tolerance in a germplasm collection of wheat (Triticum spp.). Theor Appl Genet 69:651–657CrossRefGoogle Scholar
  76. Sayed OH (2003) Chlorophyll fluorescence as a tool in cereal crop research. Photosynth 41:321–330CrossRefGoogle Scholar
  77. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62CrossRefGoogle Scholar
  78. Sharma PK, Varma SK, Datta KS, Kumar B (1992) Salinity effects on some morpho-physiological water relations and mineral composition characteristics of two cultivars of wheat with varying salt resistance. Ann Biol 10:39–50Google Scholar
  79. Shaw RJ (1999) Soil salinity- electrical conductivity and chloride. In: Peverill KI, Sparrow LA, Reuter DJ (eds) Soil Analysis: an interpretation manual. CSIRO, Collingwood, pp 129–146Google Scholar
  80. Singh SP, Verma SK, Singh RK, Pandey PK (1989) Copper uptake by free and immobilized cyanobacterium. FEMS Microbiol Lett 60:193–196CrossRefGoogle Scholar
  81. Sood A, Singh PK, Kumar A, Singh R, Prasanna R (2011) Growth and biochemical characterization of associations between cyanobionts and wheat seedlings in co-culturing experiments. Biologia 66:104–110CrossRefGoogle Scholar
  82. Subhashini D, Kaushik BD (1981) Amelioration of sodic soils with blue-green algae. Aust J Soil Res 19:361–366CrossRefGoogle Scholar
  83. Svircev Z, Tamas I, Nenin P, Drobac A (1997) Co-cultivation of N2-fixing cyanobacteria and some agriculturally important plants in liquid and sand cultures. Appl Soil Ecol 6:301–308CrossRefGoogle Scholar
  84. Tanji KK (1990) Nature and extent of agricultural salinity. In: Tanji KK (ed.) Agricultural salinity assessment and management, ASCE Manuals and reports on engineering practice No. 71, American society of civil engineers, New York, pp 1–17Google Scholar
  85. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527PubMedCrossRefGoogle Scholar
  86. Vaishamayan A, Sinha RP, Hader D-P, Dey T, Gupta AK, Bhan U, Rao AL (2001) Cyanobacterial biofertilizers in rice agriculture. Bot Rev 67:453–516CrossRefGoogle Scholar
  87. van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 2:147–150CrossRefGoogle Scholar
  88. Veluci RM, Neher DA, Weicht TR (2006) Nitrogen fixation and leaching of biological soil crust communities in mesic temperate soils. Microbial Ecol 51:189–196CrossRefGoogle Scholar
  89. Woo NS, Badger MR, Pogson BJ (2008) A rapid, non-invasive procedure for quantitative assessment of drought survival using chlorophyll fluorescence. Plant Meth. doi: 10.1186/1746-4811-4-27
  90. Yang Y, Xu S, Li A, Chen N (2007) NADPH oxidase-dependent hydrogen peroxide production, induced by salinity stress, may be involved in the regulation of total calcium in roots of wheat. J Plant Physiol 164:1429–1435PubMedCrossRefGoogle Scholar
  91. Yee N, Benning LG, Phoenix VR, Ferris FG (2004) Characterization of metal-cyanobacteria sorption reactions: a combined macroscopic and infrared spectroscopic investigation. Environ Sci Technol 38:775–782PubMedCrossRefGoogle Scholar
  92. Zheng Y, Jia A, Ning T, Xu J, Li Z, Jiang G (2008) Potassium nitrate application alleviates sodium chloride stress in winter wheat cultivars differing in salt tolerance. J Plant Physiol 165:1455–1465PubMedCrossRefGoogle Scholar
  93. Zhu J-K (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.NSW Department of Primary IndustriesElizabeth Macarthur Agricultural InstituteMenangleAustralia
  2. 2.School of Biotechnology and Biomolecular SciencesUniversity of New South WalesSydneyAustralia
  3. 3.Royal Botanic Gardens and Domain TrustSydneyAustralia
  4. 4.Department of Plant Ecology and SystematicsTechnical University of KaiserslauternKaiserslauternGermany

Personalised recommendations