COMBINED APPLICATION OF ARBUSCULAR MYCORRHIZAE FUNGI AND PLANT GROWTH PROMOTING BACTERIA IMPROVES GROWTH AND NUTRIENT UPTAKE EFFICIENCY OF PEA (PISUM SATIVUM L.) PLANTS

Eriola Veselaj; Glenda Sallaku; Astrit Balliu

doi:10.24326/asphc.2018.5.7

Tom 17 Nr 5 (2018)

Artykuły

COMBINED APPLICATION OF ARBUSCULAR MYCORRHIZAE FUNGI AND PLANT GROWTH PROMOTING BACTERIA IMPROVES GROWTH AND NUTRIENT UPTAKE EFFICIENCY OF PEA (PISUM SATIVUM L.) PLANTS

Eriola Veselaj⁺⁻
Glenda Sallaku⁺⁻
Astrit Balliu⁺⁻

PDF (English)

DOI: https://doi.org/10.24326/asphc.2018.5.7
Przesłane: 29 listopada 2018
Opublikowane: 2018-11-29

Abstrakt

The study aimed to investigate the effects of commercially available AMF inoculate (a mixture of Rhizophagus intraradices, Claroideoglomus etunicatum, Funneliformis mossea, Funneliformis geosporum, Rhizophagus clarus) and plant growth promoting bacteria (Rhizobium leguminosarum and Burkholderia sp.), either supplied individually or in combination with each other, on growth, root morphology and nutrient uptake capabilities in field pea (Pisum sativum L.) plants. Inoculated and non-inoculated pea plants were subjected to three levels of salinity (0, 20 and 50 mM) by the addition of sodium chloride into tap water. Morphology of root system was analyzed and dry matter of roots and shoots were individually measured several times during the growing cycle in randomly selected plants. The dry matter of roots and shoots was mixed together and concentration of N, P, K and Na was analytically determined. The raise of salinity in the irrigation water has strongly diminished the growth of pea plants by significantly reducing the weight, length, and surface area of root system, and deteriorating its nutrient capabilities. The inoculation of either AM fungi or PGPB in the growing substrate has contributed to alleviating the salinity stress effects through promoting growth and enhancing nutrient uptake capabilities of the root system. The combined application of AM fungi and PGPB could further enhance the nutrient uptake capabilities of pea plants under adverse salinity conditions.

Bibliografia

Abdel Latef, A.A.H., Chaoxing, H. (2011). Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci. Hortic., 127, 228–233.
Abeer, H., Alqarawi, A.A., Mona, A. (2015). Arbuscular mycorrhizal fungi mitigates NaCl induced adverse effects on Solanum lycopersicum L. Pak. J. Bot., 47(1), 327–340.
Al-Karaki, G.N. (2000). Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza, 10(2), 51–54.
Aloni, B., Karni, L., Deventurero, G., Cohen, R., Katzir, N., Edelstein M., Aktas H. 2011. The use of plant grafting and plant growth regulators for enhancing abiotic stress tolerance in vegetable transplants. Acta Hortic., 828, 255–264.
Babaj, I., Sallaku, G., Balliu, A. (2014). The effects of endogenous mycorrhiza (Glomus sp.) on plant growth and yield of grafted cucumber (Cucumis sativum L.) under common commercial greenhouse conditions. Albanian J. Agric. Sci., 13(2), 24–28.
Balliu, A., Bani, A., Sulçe, S. (2007). Nitrogen effects in the relative growth rate and its components of pepper (Capsicum annum L.) and eggplant (Solanum melongena L.) seedlings. Acta Hortic., 747, 257–262.
Balliu, A., Sallaku, G., Rewald, B. (2015). AMF inoculation enhances growth and improves the nutrient uptake rates of transplanted, salt-stressed tomato seedlings. Sustainability, 7, 15967–15981.
Bona, E., Lingua, G., Manassero, P., Cantamessa, S., Marsano, F., Todeschini, V., Copetta, A., Agostino, G.D., Massa, N., Avidano, L., Gamalero, E., Berta, G. (2015). AM fungi and PGP pseudomonads increase flowering, fruit production, and vitamin content in strawberry grown at low nitrogen and phosphorus levels. Mycorrhiza, 25, 181–193.
Cuartero, J., Bolarín, M.C., Asíns, M.J., Moreno, V. (2006). Increasing salt tolerance in the tomato. J. Exp. Bot., 57(5), 1045–1058.
Edelstein, M., Plaut, Z., Ben-Hur, M. (2011). Sodium and chloride exclusion and retention by non-grafted and grafted melon and cucurbita plants. J. Exp. Bot., 62(1), 177–184.
Egamberdieva, D., Jabborova, D., Wirth S. (2013). Alleviation of salt stress in legumes by co-inoculation with Pseudomonas and Rhizobium. In: Plant microbe symbiosis: fundamentals and advances, Arora, N.K. (ed.). Springer, New Delhi.
Ekinci, M., Turan, M., Yildirim, E., Güne, A., Kotan, R., Dursun, A. (2014). Effects of plant growth promoting rhizobacteria on growth, nutrient, organic acid, aminoacid and hormone content of cauliflower (Brassica oleracea L. var. botrytis) transplant. Acta Sci. Pol. Hortorum Cultus, 13(6), 71–85.
Estañ, M.T., Martinez-Rodriguez, M.M., Perez-Alfocea, F., Flowers, T.J., Bolarin, M.C. (2005). Grafting raises the salt tolerance of tomato through limiting the transport of sodium and chloride to the shoot. J. Exp. Bot., 56(412), 703–712.
Evelin, H., Giri, B., Kapoor, R. (2012). Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza, 22(3), 203–217.
Evelin, H., Kapoor, R., Giri, B. (2009). Arbuscular mycorrhizal fungi in alleviation of salt stress: A review. Ann. Bot., 104(7), 1263–1280.
Flowers, T.J. (2004). Improving crop salt tolerance. J. Exp. Bot., 55(396), 307–319.
Gamalero, E., Glick, B.R. (2014). Mechanisms used by plant growth-promoting bacteria. In: Bacteria in agrobiology: plant nutrient management, Maheshwari, D.K. (ed.) Springer-Verlag, Berlin–Heidelberg.
Gomes, M.A.D.C., Suzuki, M.S., Da Cunha, M., Tullii, C.F. (2011). Effect of salt stress on nutrient concentration, photosynthetic pigments, proline and foliar morphology of Salvinia auriculata Aubl. Acta Limnol. Bras., 23(2), 164–176.
Havugimana, E., Bhople, B.S., Byiringiro, E., Mugabo, J.P. (2016). Role of dual inoculation of Rhizobium and arbuscular mycorrhizal (AM) fungi on pulse crops production. Walailak J. Sci. Technol., 13(1), 1–7.
Himmelbauer, M.L., Loiskandl, W., Kastanek, F. (2004). Estimating length, average diameter and surface area of roots using two different Image analyses systems. Plant Soil, 260(1–2), 111–120.
Huang, Y., Zhu, J., Zhen, A., Chen, L., Bie, Z. (2009). Organic and inorganic solutes accumulation in the leaves and roots of grafted and ungrafted cucumber plants in response to NaCl stress. J. Food Agric. Environ., 7(2), 703–708.
Jahromi, F., Aroca, R., Porcel, R., Ruiz-Lozano, J.M. (2008). Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microbiol. Ecol., 55(1), 45–53.
Liu, W., Baddeley, J., Watson, Ch. (2011). Models of biological nitrogen fixation of legumes. A review. Agron. Sust. Dev., 31 (1), 155–172.
Martinez, V., Del Amor, F.M., Marcelis, L.F.M., (2005). Growth and physiological response of tomato plants to different periods of nitrogen starvation and recovery. J. Hortic. Sci. Biotechnol., 80, 147–153.
Meça, E., Sallaku, G., Balliu, A. (2016). Artificial inoculation of AM fungi improves nutrient uptake efficiency in salt stressed pea (Pissum sativum L.) plants. J. Agric. Stud., 4(3), 37–46.
Meça, E., Sallaku, G., Balliu, A. (2017). Could the artificial inoculation of AM fungi improve the benefits of using pea (Pisum sativum L.) plants for soil amendment purposes in greenhouses? Acta Hortic., 1164, 233–240.
Mmbaga, G.W., Mtei, K.M., Ndakidemi, P.A. (2014). Extrapolations on the use of rhizobium inoculants supplemented with phosphorus (P) and potassium (K) on growth and nutrition of legumes. Agric. Sci., 5, 1207–1226.
Munns, R., 2002. Comparative physiology of salt and water stress. Plant Cell Environ., 25(2), 239–250.
Niu, Y.F., Chai, R.S., Jin, G.L., Wang, H., Tang, C.X., Zhang, Y.S. (2013). Responses of root architecture development to low phosphorus availability: A review. Ann. Bot. 112(2), 391–408.
Peix, A., Ramírez-Bahena, M.H., Velázquez, E., Bedmar, E. J. (2014). Bacterial associations with legumes. Crit. Rev. Plant Sci., 34(1–3), 17–42.
Peng, Y., Niklas, K.J., Sun, S. (2011). The relationship between relative growth rate and whole-plant C: N: P stoichiometry in plant seedlings grown under nutrient-enriched conditions. J. Plant Ecol., 4(3), 147–156.
Porcel, R., Aroca, R., Azcon, R., Ruiz-Lozano, J.M. (2016). Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza, 26(7), 673–684. DOI 10.1007/s00572-016-0704-5.
Porcel, R., Aroca, R., Ruiz-Lozano, J.M. (2012). Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sustain. Dev., 32, 181–200.
Rewald, B., Holzer, L., Göransson, H. (2015). Arbus- cular mycorrhiza inoculum reduces root respiration and improves biomass accumulation of salt-stressed Ulmus glabra seedlings. Urban For. Urban Green., 14, 432–437.
Ruiz-Lozano, J.M., Azcón, R. (2000). Symbiotic efficiency and infectivity of an autochthonous arbuscular mycorrhizal Glomus sp. from saline soils and Glomus deserticola under salinity. Mycorrhiza, 10, 137–143.
Pięta, D., Pastucha, A. (2008). Antagonistic bacteria and their post culture liquids in the protection of pea (Pisum sativum L.) from diseases. Acta Sci. Pol. Hortorum Cultus, 7(4), 31–42.
Shelden, M.C., Roessner, U. (2013). Advances in functional genomics for investigating salinity stress tolerance mechanisms in cereals. Front. Plant Sci., 4, 123. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3650683&tool=pmcentrez&rendertype=abstract.
Vuksani, A., Sallaku, G., Balliu, A. (2015). The effects of endogenous mycorrhiza (Glomus sp.) on stand establishment rate and yield of open field tomato crop. Albanian J. Agric. Sci., 14(1), 25–30.
Wakeel, A., 2013. Potassium – sodium interactions in soil and plant under saline-sodic conditions. J. Plant Nutr. Soil Sci., 176, 344–354.

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Słowa kluczowe

AMF
Rhizobium leguminosarum
Burkholderia sp.
salinity
dry matter
root length
root surface area
nutrient uptake rate

Prawa autorskie

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[1] Abdel Latef, A.A.H., Chaoxing, H. (2011). Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci. Hortic., 127, 228–233.

[2] Abeer, H., Alqarawi, A.A., Mona, A. (2015). Arbuscular mycorrhizal fungi mitigates NaCl induced adverse effects on Solanum lycopersicum L. Pak. J. Bot., 47(1), 327–340.

[3] Al-Karaki, G.N. (2000). Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza, 10(2), 51–54.

[4] Aloni, B., Karni, L., Deventurero, G., Cohen, R., Katzir, N., Edelstein M., Aktas H. 2011. The use of plant grafting and plant growth regulators for enhancing abiotic stress tolerance in vegetable transplants. Acta Hortic., 828, 255–264.

[5] Babaj, I., Sallaku, G., Balliu, A. (2014). The effects of endogenous mycorrhiza (Glomus sp.) on plant growth and yield of grafted cucumber (Cucumis sativum L.) under common commercial greenhouse conditions. Albanian J. Agric. Sci., 13(2), 24–28.

[6] Balliu, A., Bani, A., Sulçe, S. (2007). Nitrogen effects in the relative growth rate and its components of pepper (Capsicum annum L.) and eggplant (Solanum melongena L.) seedlings. Acta Hortic., 747, 257–262.

[7] Balliu, A., Sallaku, G., Rewald, B. (2015). AMF inoculation enhances growth and improves the nutrient uptake rates of transplanted, salt-stressed tomato seedlings. Sustainability, 7, 15967–15981.

[8] Bona, E., Lingua, G., Manassero, P., Cantamessa, S., Marsano, F., Todeschini, V., Copetta, A., Agostino, G.D., Massa, N., Avidano, L., Gamalero, E., Berta, G. (2015). AM fungi and PGP pseudomonads increase flowering, fruit production, and vitamin content in strawberry grown at low nitrogen and phosphorus levels. Mycorrhiza, 25, 181–193.

[9] Cuartero, J., Bolarín, M.C., Asíns, M.J., Moreno, V. (2006). Increasing salt tolerance in the tomato. J. Exp. Bot., 57(5), 1045–1058.

[10] Edelstein, M., Plaut, Z., Ben-Hur, M. (2011). Sodium and chloride exclusion and retention by non-grafted and grafted melon and cucurbita plants. J. Exp. Bot., 62(1), 177–184.

[11] Egamberdieva, D., Jabborova, D., Wirth S. (2013). Alleviation of salt stress in legumes by co-inoculation with Pseudomonas and Rhizobium. In: Plant microbe symbiosis: fundamentals and advances, Arora, N.K. (ed.). Springer, New Delhi.

[12] Ekinci, M., Turan, M., Yildirim, E., Güne, A., Kotan, R., Dursun, A. (2014). Effects of plant growth promoting rhizobacteria on growth, nutrient, organic acid, aminoacid and hormone content of cauliflower (Brassica oleracea L. var. botrytis) transplant. Acta Sci. Pol. Hortorum Cultus, 13(6), 71–85.

[13] Estañ, M.T., Martinez-Rodriguez, M.M., Perez-Alfocea, F., Flowers, T.J., Bolarin, M.C. (2005). Grafting raises the salt tolerance of tomato through limiting the transport of sodium and chloride to the shoot. J. Exp. Bot., 56(412), 703–712.

[14] Evelin, H., Giri, B., Kapoor, R. (2012). Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza, 22(3), 203–217.

[15] Evelin, H., Kapoor, R., Giri, B. (2009). Arbuscular mycorrhizal fungi in alleviation of salt stress: A review. Ann. Bot., 104(7), 1263–1280.

[16] Flowers, T.J. (2004). Improving crop salt tolerance. J. Exp. Bot., 55(396), 307–319.

[17] Gamalero, E., Glick, B.R. (2014). Mechanisms used by plant growth-promoting bacteria. In: Bacteria in agrobiology: plant nutrient management, Maheshwari, D.K. (ed.) Springer-Verlag, Berlin–Heidelberg.

[18] Gomes, M.A.D.C., Suzuki, M.S., Da Cunha, M., Tullii, C.F. (2011). Effect of salt stress on nutrient concentration, photosynthetic pigments, proline and foliar morphology of Salvinia auriculata Aubl. Acta Limnol. Bras., 23(2), 164–176.

[19] Havugimana, E., Bhople, B.S., Byiringiro, E., Mugabo, J.P. (2016). Role of dual inoculation of Rhizobium and arbuscular mycorrhizal (AM) fungi on pulse crops production. Walailak J. Sci. Technol., 13(1), 1–7.

[20] Himmelbauer, M.L., Loiskandl, W., Kastanek, F. (2004). Estimating length, average diameter and surface area of roots using two different Image analyses systems. Plant Soil, 260(1–2), 111–120.

[21] Huang, Y., Zhu, J., Zhen, A., Chen, L., Bie, Z. (2009). Organic and inorganic solutes accumulation in the leaves and roots of grafted and ungrafted cucumber plants in response to NaCl stress. J. Food Agric. Environ., 7(2), 703–708.

[22] Jahromi, F., Aroca, R., Porcel, R., Ruiz-Lozano, J.M. (2008). Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microbiol. Ecol., 55(1), 45–53.

[23] Liu, W., Baddeley, J., Watson, Ch. (2011). Models of biological nitrogen fixation of legumes. A review. Agron. Sust. Dev., 31 (1), 155–172.

[24] Martinez, V., Del Amor, F.M., Marcelis, L.F.M., (2005). Growth and physiological response of tomato plants to different periods of nitrogen starvation and recovery. J. Hortic. Sci. Biotechnol., 80, 147–153.

[25] Meça, E., Sallaku, G., Balliu, A. (2016). Artificial inoculation of AM fungi improves nutrient uptake efficiency in salt stressed pea (Pissum sativum L.) plants. J. Agric. Stud., 4(3), 37–46.

[26] Meça, E., Sallaku, G., Balliu, A. (2017). Could the artificial inoculation of AM fungi improve the benefits of using pea (Pisum sativum L.) plants for soil amendment purposes in greenhouses? Acta Hortic., 1164, 233–240.

[27] Mmbaga, G.W., Mtei, K.M., Ndakidemi, P.A. (2014). Extrapolations on the use of rhizobium inoculants supplemented with phosphorus (P) and potassium (K) on growth and nutrition of legumes. Agric. Sci., 5, 1207–1226.

[28] Munns, R., 2002. Comparative physiology of salt and water stress. Plant Cell Environ., 25(2), 239–250.

[29] Niu, Y.F., Chai, R.S., Jin, G.L., Wang, H., Tang, C.X., Zhang, Y.S. (2013). Responses of root architecture development to low phosphorus availability: A review. Ann. Bot. 112(2), 391–408.

[30] Peix, A., Ramírez-Bahena, M.H., Velázquez, E., Bedmar, E. J. (2014). Bacterial associations with legumes. Crit. Rev. Plant Sci., 34(1–3), 17–42.

[31] Peng, Y., Niklas, K.J., Sun, S. (2011). The relationship between relative growth rate and whole-plant C: N: P stoichiometry in plant seedlings grown under nutrient-enriched conditions. J. Plant Ecol., 4(3), 147–156.

[32] Porcel, R., Aroca, R., Azcon, R., Ruiz-Lozano, J.M. (2016). Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza, 26(7), 673–684. DOI 10.1007/s00572-016-0704-5.

[33] Porcel, R., Aroca, R., Ruiz-Lozano, J.M. (2012). Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sustain. Dev., 32, 181–200.

[34] Rewald, B., Holzer, L., Göransson, H. (2015). Arbus- cular mycorrhiza inoculum reduces root respiration and improves biomass accumulation of salt-stressed Ulmus glabra seedlings. Urban For. Urban Green., 14, 432–437.

[35] Ruiz-Lozano, J.M., Azcón, R. (2000). Symbiotic efficiency and infectivity of an autochthonous arbuscular mycorrhizal Glomus sp. from saline soils and Glomus deserticola under salinity. Mycorrhiza, 10, 137–143.

[36] Pięta, D., Pastucha, A. (2008). Antagonistic bacteria and their post culture liquids in the protection of pea (Pisum sativum L.) from diseases. Acta Sci. Pol. Hortorum Cultus, 7(4), 31–42.

[37] Shelden, M.C., Roessner, U. (2013). Advances in functional genomics for investigating salinity stress tolerance mechanisms in cereals. Front. Plant Sci., 4, 123. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3650683&tool=pmcentrez&rendertype=abstract.

[38] Vuksani, A., Sallaku, G., Balliu, A. (2015). The effects of endogenous mycorrhiza (Glomus sp.) on stand establishment rate and yield of open field tomato crop. Albanian J. Agric. Sci., 14(1), 25–30.

[39] Wakeel, A., 2013. Potassium – sodium interactions in soil and plant under saline-sodic conditions. J. Plant Nutr. Soil Sci., 176, 344–354.