Effect of Ectomycorrhizal fungi symbiosis and mycorrhiza helper bacteria (Bacillus cereus) on nutrient uptake and growth of Black pine (Pinus nigra)

Document Type : scientific research article

Authors

1 Ph.D. Student, Dept. of Horticulture, Faculty of Agriculture Science, University of Guilan, Rasht, Iran

2 Professor, Dept. of Horticulture, Faculty of Agriculture Science, University of Guilan, Rasht, Iran

3 Associate Prof., Dept. of Horticulture, Faculty of Agriculture Science, University of Guilan, Rasht, Iran

4 Assistant Prof., Dept. of Plant Protection, Faculty of Agriculture Science, University of Guilan, Rasht, Iran

Abstract

Background and Objectives: Mycorrhiza is one of the most common and oldest symbiotic associations in the plants. These funguses are considered to be essential factors in the soil and plant system which symbiosis with roots of more than 97% of the plants. Nowadays it is known that mycorrhizal fungus increase host plant growth by in direct ways such as improving plant nutrition by absorbing nutrients, as well as increasing water absorption and indirect way such as reducing biologic and non-biologic stress. Pine trees are the most popular trees in the landscape and forests, which have compulsory symbiosis with ectomycorrhizal fungi. Several studies have been done to development symbiosis of ectomycorrhiza in sterile conditions, as well as to investigate the effect of this system on plants, but so far no studies have been done to investigate the symbiosis of three types of ectomycorrhizal fungi (Cantharellus cibarius, Amanita caesarea and Boletus edulis) and bacteria (Bacillus cereus) with black pine.
Materials and methods: This experiment was conducted in a completely randomized design with three replications. The treatments were included: Control, B. cereus, the ectomycorrhiza funguses of Cantharellus, Boletus and Amanita and combined treatments (bacterial+ fungi). Seedlings were inoculated with fungi and bacteria after 60 days; then, the traits were evaluated after 15 months. The traits were included: root mycorrhization percent, plant height, stem diameter, stem and root dry weight, chlorophyll content and the uptake of nitrogen, phosphorus, potassium and calcium.
Results: Mycorrhization at 1% probability was significantly influenced by applied treatments. The highest (61.32%) and lowest (14%) percentage of mycorrhization respectively were obtained by Boletus+Bacillus and Cantharellus. The uptake of potassium, nitrogen and phosphorus elements, Atotal chlorophyll, plant height and root and stem dry weight were significantly affected by treatments; while, there were not observed significant difference between treatments in case of stem diameter, calcium uptake and chlorophyll b. All combination treatments (bacterial+fungi) dramatically increased plant height, stem dry weight, total chlorophyll and the absorption of potassium and nitrogen compared with control. Also the treatments of Boletus+Bacillus and Amanita+Bacillus had positivity effects on increment of phosphorus uptake, Chlorophyll a and root dry weight. In case of individual treatments, the results showed that only Boletus was effective in improving the stem dry weight and potassium and phosphorus uptake. In the case of separate treatments, the results indicated that only Boletus fungus was effective in increasing stem dry weight and potassium and phosphorus absorption. In other case there were no significant difference between control and other treatments. The highest and lowest values of evaluated traits respectively were obtained by Boletus+Bacillus and control.
Conclusion: The results conclusively suggest that all ectomycorrhizal fungus especially Boletus had a symbiosis with P. nigra. This symbiosis was improved by mycorrhiza helper bacteria and co-inoculated of B. cereus with all fungi had more positive effects on increasing of mycorrhization, nutrient uptake and growth of P. nigra.

Keywords


1.Aghababaei, F., Raiesi, F. and Nadian, H. 2011. Influence of mycorrhizal symbiosis on the uptake of nutrients in some commercial genotypes of almond ina sandy loam soil. Iran. J. Soil Res.25: 2. 137-147. (In Persian)
2.Ahangar, M.A., Dar, G.H. and Bhat, Z.A. 2012. Growth response and nutrient uptake of blue pine (Pinus wallichiana ) seedlings inoculated with rhizosphere microorganisms under temperate nursery conditions. Ann. Sci. 55: 2. 217-227.
3.Arnon, D. 1956. Photosynthesis by isolated chloroplast. Arch. Biochem. Biophys. 20: 3. 449-461.
4.Aspray, T.J., Frey-Klett, P., Jones, J.E., Whipps, J.M., Garbaye, J. and Bending, G.D. 2006. Mycorrhization helper bacteria: a case of specificity for altering ectomycorrhiza architecture but not ectomycorrhiza formation. Mycorrhiza. 16: 8. 533-541.
5.Bago, B., Pfeffer, P.E. and Shachar-Hill, Y. 2000. Carbon metabolism and transport in Arbuscular mycorrhizas. Plant Physiol. 124: 3. 949-958.
6.Berg, B. and Mclaugherty, C. 2004. Plant litter: decomposition, humus formation, carbon sequestration. Springer Verlag, Berlin. Plant Physiol. 161. 10. 1185-1188.
7.Bertrand, H., Plassard, C., Pinochet, X., Touraine, B., Normand, P. and Cleyet Marcel, J.C. 2000. Stimulation of the conic transport system in Brassicanapus by a plant growth promoting rhizobacterium (Achromobacter sp.).Can. J. Microbiol. 46: 3. 229-236.
8.Brundrett, M.C. 2009. Mycorrhizal associations and other means of nutrition of vascular plants; understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil. 320: 1-2. 37-77.
9.Brzostek, E.R., Greco, A., Drake, J.E. and Finzi, A.C. 2013. Root carbon inputs to the rhizospher estimulate extra cellular enzyme activity and increase nitrogen availability in temperate forest soils. Biogeochemistry. 115: 1-3. 65-76.
10.Cui, Y.Y., Feng, B., Wu, G., Xu, J. and Yang, Zh. 2016. Porcini mushrooms (Boletus sect. Boletus) from China. Fungal Divers. 81: 1. 189-212.
11.Dentinger, B.T. and Suz, L.M. 2014. What’s for dinner? Undescribed species of porcini in a commercial packet. Peer J. DOI: 10.7717/peerj.570.
12.Dong, C., Hu, D., Fu, Y., Wang, M. and Liu, H. 2014. Analysis and optimization of the effect of light and nutrient solution on wheat growth and development using an inverse system model strategy. Comput. Electron. Agric. 109: 3. 221-231.
13.Duponnois, R. and Plenchette, C. 2003. A mycorrhiza helper bacterium enhances ectomycorrhizal and endomycorrhizal symbiosis of Australian Acacia species. Mycorrhiza. 13: 2. 85-91.
14.Farahmand, H. 2015. Trees and ornamental shrubs (Gymnosperms). Mashhad University Press. 459p.(In Persian)
15.Frey-Klett, P., Garbaye, J. andTarkka, M. 2007. The mycorrhizahelper bacteria revisited. New Phytol. 176: 1. 22-36.
16.Garbay, J. and Duponnois, R. 1992. Specifi city and function of mycorrhization helper bacteria (MHB) associated with the Pseudotsuga menziesii-Lacacria laccata symbiosis. Symbiosis. 14: 1. 335-344.
17.Hamel, C.A. and Smith, D.L. 1991. Interspecific N-transfer and plant development in mycorrhiza field-grown moisture. Soil Biol. Biochem.23: 1. 661-665.
18.Hill, D. 2012. Truffles and other edible mycorrhiza mushrooms. Reported by College of Agriculture, Food and Environment of University of Kentucky. https://www.uky.edu/Ag/CCD/introsheets/truffles.pdf.
19.Kafi, M., Daneshvar Hakimi Meybodi, N., Nikbakht, A., Rejali, F. and Daneshkhah, M. 2013. Effect of humic acid and mycorrhiza fungi on some characteristics of “Speedy green” perennial ryegrass (Lolium perenne L.). greenhouse cultivation. Sci and Techno greenhouse cult. 4: 13. 49-58. (In Persian)
20.Kayama, M. and Yamanaka, T.2016. Growth characteristics of ectomycorrhizal seedlings of Quercus glauca, Quercus salicina, Quercus myrsinaefolia, and Castanopsis cuspidata planted in calcareous Soil. Forests.7: 11. 266.
21.Laiye, Q.U., Quoreshi, A.M., Iwase, K., Tamai, Y., Funada, R. and Koike, T. 2003. In vitro ectomycorrhizal formation on two larch species of seedlings with six different fungal species. Eurasiana. Eurasian J. For. Res. 6: 1. 65-73.
22.Leyval, C. and Berthelin, J. 1990. Influence of acid producing agrobacterium and Laccaria laccata on pine and beech growth, nutrient uptake and exudation. Agric. Ecosyst. Environ. 28: 1-4. 313-319.
23.Lu, N., Yu, M., Cui, M., Luo, Z., Feng, Y., Cao, S., Sun, Y. and Li, Y. 2016. Effects of different ectomycorrhizal fungal inoculates on the growth of Pinus tabulaeformis seedlings under greenhouse conditions. Forests. 7: 12. 316.
24.Martin, T., Oswald, O. and Graham,I.A. 2002. Arabidopsis seedling growth, storage lipid mobilization and photosynthetic gene expression are regulated by carbon: Nitrogen availability. Plant Physiol. 128: 2. 472-481.
25.Martins, A. 2008. In vitro mycorrhization of micropropagated plants: Studies on castanea sativa mill. Siddiqui Z.A., Akhtar M.S. and Futai K. (Eds.). Mycorrhiza: J. Sust. Agric. Springer. pp. 319-334.
26.Mcpartland, J.M., Robert, C.C. and Watson, D.P. 2000. Hemp diseases and pests: management and biological control: an advanced treatise. CABI Publishing, Wallingford, 506p.
27.Mediavilla, O., Olaizola, J., Santos-del-Blanco, L., Oria-de-Rueda, J.A. and Martín-Pinto, P. 2016. Mycorrhization between Cistus ladanifer L. and Boletus edulis Bull is enhanced by the mycorrhiza helper bacteria pseudomonas fluorescens Migula. Mycorrhiza.26: 2. 161-168.
28.Mozaffarian, V. 2004. Trees and shrubs of Iran, Farhang-e-Moaser Publishing. 214p. (In Persian)
29.Olfati, J., Peyvast, Gh. and Mami, Y. 2009. Identification and chemical properties of popular wild edible mushrooms from northern Iran. J. Hortic. For. 1: 3. 48-51.
30.Olsen S.R. and Sommers, L.E. 1982. Methods of soil analysis, part 2, chemical and microbiological properties. Soil Sci. Soc. pp. 403-430.
31.Polanco, M.C., Zwiazek, J.J. andVoicu, M.C. 2008. Responses of ectomycorrhizal American Elm (Ulmus americana) seedlings to salinity and soil compaction. Plant Soil. 308: 1. 189-200.
32.Postgate, J.R. 1982. Biological nitrogen fixation: fundamentals. Philos. Trans. R Soc. Lond B Biol. Sci. 296: 375-385.
33.Sadaghiani, M.R., Gharemaleki, T., Besharati, H. and Tavasolee, A. 2011. Effects of PGPR and AM fungi on growth and Zn uptake by Corn Plant in a Zn- contaminated Soil. Water Soil Sci. 21: 2. 136-147. (In Persian)
34.Sheng, J.M., Wu, X.Q., Hou, L.L.and Ying, C.X. 2010. Isolation and identification of a MHB strain from the rhizosphere soil of Pinus thunbergi inoculated with Boletus edulis Environ. Biol. 16: 5. 701-704.
35.Sitta, N. and Davoli, P. 2012. Edible ectomycorrhizal mushrooms: international markets and regulations. Edible ectomycorrhizal mushrooms. Springer. Soil Biol. 34: 355-380.
36.Smith, S.E. and Read, D.J. 2008. Mycorrhizal symbiosis, thirded. Academic Press, London, UK. 800p.
37.Smith, S.E. 2003. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol. 133: 1. 16-20.
38.Turgeman, T., Asher, J.B., Roth-Bejerano, N., KaganZur, V., Kapulnik, Y. and Sitrit, Y. 2011. Mycorrhizal association between the desert truffle Terfezia boudieri and Helianthemum sessiliflorum alters plant physiology and fitness to arid conditions. Mycorrhiza. 21: 623-630.
39.Turk, M.A., Assaf, T.A., Hameed,K.M. and Tawaha, A.M. 2006. Significance of mycorrhizae. World. Agric. Sci. 2: 1. 16-20.
40.Van Aarle, I.M., Olsson, P.A. and Soderstrom, B. 2001. Microscopic detection of phosphatase activity of saprophytic and arbuscular mycorrhizal fungi using a fluorogenic substrate. Mycol Iran. 93: 1. 17-24.
41.Vodnik, D. and Gogala, N. 1994. Seasonal fluctuations of photosynthesis and its pigments in 1-year mycorrhized spruce seedlings. Mycorrhiza. 4: 6. 277-281.
42.Wu, X.Q., Hou, L.L., Sheng, J.M., Ren, J.H., Zheng, L., Chen, D. and Ye, J.R. 2012. Effects of ectomycorrhizal fungus Boletus edulis and mycorrhiza helper Bacillus cereus on the growth and nutrient uptake by Pinus thunbergii. Biol Fertil Soil. 48: 4. 385-391.
43.Zamani, S.M., Mohamadi Goltapeh, E., Safaey, N. and Emam, M. 2015. Effect of ectomycorrhizal symbiosis on the growth and physiology of Quercus castaneifolia C. A. Mey. plantlets.Iran. J. Forest. Range Protec. Res.13: 2. 160-170. (In Persian)
44.Zhang, L., Yang, J. and Yang, Z.2004. Molecular phylogeny ofeastern Asian species of Amanita (Agaricales, Basidiomycota): taxonomic and biogeographic implications. Fungal Divers. 17: 219-238.