USE OF PLANT GROWTH PROMOTING RHIZOBACTERIA AGAINST SALT STRESS FOR TOMATO (Solanum lycopersicum L.) SEEDLING GROWTH
Yagmur Yilmaz
The Institute of Natural & Applied Sciences, Van Yuzuncu Yil University 65080 Van, Turkeyhttps://orcid.org/0000-0002-0769-9171
Ceknas Erdinc
Agricultural Biotechnology Department, Agriculture Faculty, Van Yuzuncu Yil University 65080 Van, Turkeyhttps://orcid.org/0000-0003-1208-032X
Ahmet Akkopru
Plant Protection Department, Agriculture Faculty, Van Yuzuncu Yil University 65080 Van, Turkeyhttps://orcid.org/0000-0002-1526-6093
Selma Kipcak
Baskale Vocational School, Van Yuzuncu Yil University, 65080 Van, Turkeyhttps://orcid.org/0000-0002-0563-1130
Abstract
Salt stress affects many aspects of plant metabolism and as a result, growth and yield are reduced. The aim in this study was to determine the effects of plant growth promoting rhizobacteria (PGPR) on tomato plants under salt stress. With this aim, the ‘Interland F1’ cv. and bacterial isolates of Bacillus thuringiensis CA41/1, Pseudomonas putida 18/1K, Pseudomonas putida S5/4ep, and Pseudomonas putida 30 were used. Salt application was completed in two different doses of 25 and 50 mM NaCl when seedlings reached the stage of
3 true leaves. At the end of the study, in addition to seedling development criteria, some nutrient element contents and rates (K, Ca, Na, K/Na and Ca/Na), superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase (APX) enzyme activities, malondialdehyde (MDA) and photosynthetic pigment contents were determined. In the stress environment, PGPR inoculation increased K content by up to 10%, while apart from isolate P. putida no.30, the other isolates lowered Na content by up to 18%. Additionally, 18/1K and S5/4ep isolates were identified to reduce membrane injury index by up to 97%. It was identified that CA41/1, 18/1K and S5/4ep isolates were more effective against salt stress, especially. In general, the plant tolerance levels induced by the bacteria were identified to increase with the increase in salt stress.
Keywords:
Solanum lycopersicum, PGPR, salt stress, enzyme, chlorophyll, seedling growthReferences
Agarwal, P.K., Shukla, P.S., Gupta, K., Jha, B. (2013). Bioengineering for salinity tolerance in plants: State of the art. Mol. Biotechnol., 54, 102–123. DOI: 10.1007/s12033-012-9538-3
Akköprü, A., Çakar, K., Husseini, A. (2018). Effects of endophytic bacteria on disease and growth in plants under biotic stress. YYU J. Agr. Sci., 28, 200–208. DOI: 10.29133/yyutbd.418070
Aktas, H., Dasgan, H.Y., Yetisir, H., Sari, N., Koc, S., Ekici, B., Solmaz, I., Unlu, H., Aloni, B. (2009). Variations in the response of different lines and hybrids of melon (Cucumis melo var. cantaloupensis) under salt stress. Am.-Eurasian J. Agric. Environ. Sci., 5, 485–493.
Antoun, H., Prévost, D. (2006). Ecology of plant growth promoting. In: PGPR: Biocontrol and Biofertilization, Siddiqui, Z.A. (ed.). Netherlands, Springer, pp. 1–39.
Amira, M.S., Qados, A. (2011). Effect of salt stress on plant growth and metabolism of bean plant Vicia faba (L.). J. Saudi Soc. Agric. Sci., 10(1), 7–15. DOI: 10.1016/j.jssas.2010.06.002
Argandona, M., Nieto, J.J., Iglesias-Guerra, F., Calderón, M.I., García-Estepa , R., Vargas, C. (2010). Interplay between iron homeostasis and the osmotic stress response in the halophilic bacterium Chromohalobacter salexigens. Appl. Environ. Microbiol., 76, 3575–3589. DOI: 10.1128/AEM.03136-09
Armada, E., Roldán, A., Azcon, R. (2014). Differential activity of autochthonous bacteria in controlling drought stress in native Lavandula and Salvia plants species under drought conditions in natural arid soil. Microbiol. Ecol., 67, 410–420. DOI: 10.1007/s00248-013-0326-9
Ashrafi, V., Seiedi, M.N. (2011). Influence of different plant densities and plant growth promoting rhizobacteria (PGPR) on yield and yield attributes of corn (Zea maize L.). Recent Res. Sci. Technol., 3, 63–66.
Azevedo Neto, A.D., de, Prisco, J.T., Eneas-Filho, J., Abreu, C.E.B, de, Gomes-Filho, E. (2006). Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ. Exp. Bot., 56, 87–94. DOI: 10.1016/j.envexpbot.2005.01.008
Bal, H.B., Nayak, L., Das, S., Adhya, T.K. (2013). Isolation of ACC deaminase producing PGPR from rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant Soil, 366, 93–105. DOI: 10.1007/s11104-012-1402-5
Baltruschat, H., Fodor, J., Harrach, B.D., Niemczyk, E., Barna, B., Gullner, G., Janeczko, A., Kogel, K.H. (2008). Salt tolerance barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol., 180, 501–510. DOI: 10.1111/j.1469-8137.2008.02583.x
Barka, E.A., Nowak, J., Clement, C. (2006). Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans Strain PsJN. Appl. Environ. Microb., 72, 7246–7252. DOI: 10.1128/AEM.01047-06
Bharti, N., Pandey, S.S., Barnawal, D., Patel, V.K., Kalra, A. (2016). Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci. Rep., 6, 34768. DOI: 10.1038/srep34768
Bora, T., Özaktan, H., Göre, E., Aslan, E. (2004). Biological control of Fusarium oxysporum f. sp. melonis by wettable powder formulations of the two strains of Pseudomonas putida. J. Phytopathol., 152, 471–475.
Cakmak, I., Marschner, H. (1992). Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol., 98, 1222–1227. DOI: 10.1104/pp.98.4.1222
Çulha, Ş., Çakırlar, H. (2011). The effect of salinity on plants and salt tolerance mechanisms. AKU J. Sci., 11, 11–34.
Długokęcka, E., Kacperska-Palacz, A. (1978). Re-examination of electrical conductivity method for estimation of drought injury. Biol. Plant., 20, 262–267.
Fan, S., Blake, T.G. (1994). Abscisic acid induced electrolyte leakage in woody species with contrasting ecological requirements. Physiol. Plant., 90, 414–419.
Faostat (2017). Statistic Database. Available: http://faostat.fao.org/ [date of access: 22.02.19].
Farooq, S., Azam, F. (2006). The use of cell membrane stability (CMS) technique to screen for salt tolerant wheat varieties. J. Plant. Physiol., 163, 629–637. DOI: 10.1016/j.jplph.2005.06.006
Forni, C., Duca, D., Glick, B.R. (2017). Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant Soil, 410, 335–356. DOI: 10.1007/s11104-016-3007-x
Ghoulam, C., Foursy, A., Fores, K. (2002). Effects of salt stress on growth ınorganic ıons and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars. Environ. Exp. Bot., 47, 39–50. DOI: 10.1016/S0098-8472(01)00109-5
Glick, B.R. (2014). Bacteria with ACC deaminase can promote plant growth and help to feed the World. Microbiol. Res., 169, 30–39. DOI: 10.1016/j.micres.2013.09.009
Groppa, M.D., Benavides, M.P., Zawoznik, M.S. (2012). Root hydraulic conductance, aquaporins and plant growth promoting microorganisms: A revision. Appl. Soil Ecol., 61, 247–254. DOI: 10.1016/j.apsoil.2011.11.013
Hardoim, P.R., Overbeek, L.S., van, Elsas, J.D., van (2008). Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol., 16, 463–471. DOI: 10.1016/j.tim.2008.07.008
Jamil, M., Ashraf, M., Rehman, S., Ahmad, M., Rha, E.S. (2012). Salinity induced changes in cell membrane stability, protein and RNA contents. Afr. J. Biotechnol., 11, 6476–6483. DOI: 10.5897/AJB11.2590
Jebara, S., Jebara, M., Limam, F., Aouani, M.E. (2005). Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. J. Plant Physiol., 162, 929–936. DOI: 10.1016/j.jplph.2004.10.005
Jha, Y., Subramanian, R. (2014). PGPR regulate caspase-like activity, programmed cell death, and antioxidant enzyme activity in paddy under salinity. Physiol. Mol. Biol. Plants, 20, 201–207. DOI: 10.1007/s12298-014-0224-8
Kang, S.M., Khan, A.L., Waqas, M., You, Y.H., Kim, J.H., Kim, J.G., Hamayun, M., Lee, I.J. (2014). Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J. Plant Interact., 9, 673–682. DOI: 10.1080/17429145.2014.894587
Katerji, N., Van Hoorn, J.W., Hamdy, A., Mastrorilli, M., Mou Karzel, E. (1997). Osmotic adjustment of sugar beets in response to soil salinity and its influence on stomatal conductance, growth and yield. Agric. Water Manag., 34, 57–69.
Kaymak, D.C. (2010). Potential of PGPR in agricultural innovations. In: Plant growth and health promoting bacteria, Maheshwari, D.K. (ed.). Springer-Verlag, Berlin–Heidelberg, Germany, 45–80.
King, E.O., Raney, D.E. (1954). Two simple media for the demonstration for pyocyanin and flourescens. J. Lab. Clin. Med., 44, 301–307.
Kumar, M., Sharma, S., Gupta, S., Kumar, V. (2018). Mitigation of abiotic stresses in Lycopersicon esculentum by endophytic bacteria. Environ. Sustain., 1, 71–80. DOI: 10.1007/s42398-018-0004-4
Loon, L.C. (2007). Plant responses to plant gowth-promoting rhizobacteria. Eur. J. Plant. Pathol., 119, 243–254. DOI: 10.1007/s10658-007-9165-1
Lucy, M., Reed, E., Glick, B.R. (2004). Applications of free living plant growth promoting rhizobacteria. Antonie Van Leewenhoek, 86, 1–25. DOI: 10.1023/B:ANTO.0000024903.10757.6e
Madhava Rao, K.V., Sresty, T.V.S. (2000). Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses. Plant Sci., 157, 113–128. DOI: 10.1016/S0168-9452(00)00273-9
Mayak, S., Tirosh, T., Glick, B.R. (2004). Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem., 42, 565–572. DOI: 10.1016/j.plaphy.2004.05.009
Munns, R. (2005). Genes and salt tolerance: bringing them together. New Phytol., 167, 645–663. DOI: 10.1111/j.1469-8137.2005.01487.x
Nadeem, S.M., Ahmad, M., Zahir, Z.A., Javaid, A., Ashraf, M. (2014). The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol. Adv., 32, 429–448. DOI: 10.1016/j.biotechadv.2013.12.005
Nagarajkumar, M., Bhaskaran, R., Velazhahan, R. (2004). Involvement of secondary metabolites and extracellular lytic enzymes produced by Pseudomonas fuorescens in inhibition of Rhizoctonia solani, the rice sheath blight pathogen. Microbiol. Res., 159, 73–81. DOI: 10.1016/j.micres.2004.01.005
Orsini, F., Sanoubar, R., Oztekin, G.B., Kappel, N., Tepecik, M., Quacquarelli, C., Tuzel, Y., Bona, S., Gianquinto, G. (2013). Improved stomatal regulation and ion partitioning boosts salt tolerance in grafted melon. Funct. Plant Biol., 40, 628–636. DOI: 10.1071/FP12350
Ozaktan, H., Çakır, B., Gül, A., Yolageldi, L., Akköprü, A., Fakhraei, D., Akbaba, M. (2015). Isolation and evaluation of endophytic bacteria against Fusarium Oxysporum f. sp. Cucumerinum infecting cucumber plants. Austin J. Plant Biol., 1, 1003.
Pieterse, C.M.J., Zamioudis, C., Berendsen, R.L., Weller, D.M., Van Wees, S.C.M., Bakker, P.A.H.M. (2014). Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol., 52, 347–375. DOI: 10.1146/annurev-phyto-082712-102340
Sadeghi, A., Karimi, E., Dahaji, P.A., Javid, M.G., Dalvand, Y., Askari, H. (2012). Plant growth promoting activity of an auxin and siderophore producing isolate of streptomyces under saline soil conditions. World J. Microbiol. Biotechnol., 28, 1503–1509. DOI: 10.1007/s11274-011-0952-7
Sarabi, B., Bolandnazar, S., Ghaderi, N., Ghashghaie, J. (2017). Genotypic differences in physiological and biochemical responses to salinity stress in melon (Cucumis melo L.) plants: Prospects for selection of salt tolerant landraces. Plant Physiol. Biochem., 119, 294–311. DOI: 10.1016/j.plaphy.2017.09.006
Sarma, B.K., Yadav, S.K., Singh, D.P., Singh, H.B. (2012). Rhizobacteria mediated induced systemic tolerance in plants: Prospects for abiotic stress management. In: Bacteria in Agrobiology: Stress Management, D. Maheshwari, D. (ed.). Springer, Berlin–Heidelberg, 225–238.
Sevengor, S., Yasar, F., Kusvuran, S., Ellialtioglu, S. (2011). The effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidative enzymes of pumpkin seedling. Afr. J. Agric. Res., 6, 4920–4924. DOI: 10.5897/AJAR11.668
Seymen, M., Türkmen, Ö., Dursun, A., Paksoy, M. (2014). Effects of bacteria inoculation on yield, yield components and mineral contents of tomato. Selcuk J. Agric. Food Sci., 28, 52–57.
Singh, S.K., Nene, Y.L., Reddy, M.V. (1990). Influence of crop system on Macrophomina phaseolina populations in soil. Plant Dis., 74, 812–814.
Singh, V.K., Singh, A.K., Singh, P.P., Kumar, A. (2018). Interaction of plant growth promoting bacteria with tomato under abiotic stress: A review. Agric. Ecosyst. Environ., 267, 129–140. DOI: 10.1016/j.agee.2018.08.020
Tank, N., Saraf, M. (2010). Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J. Plant Interact., 5, 51–58. DOI: 10.1080/17429140903125848
Tester, M., Davenport, R. (2003). Na+ tolerance and Na+ transport in higher plants. Ann. Bot., 91, 503–527. DOI: 10.1093/aob/mcg058
Tuteja, N., Sing, L.P., Gill, S.S., Gill, R., Tuteja, R. (2012). Improving crop resistance to abiotic stress. In: Salinity Stress: A Major Constraint in Crop Production, Tuteja, N., Gill, S., Tiburcio, A.F., Tuteja, R. (ed.). Wiley-VCH Verlag and Co. KGaA, Weinheim, Germany, 71–96.
Vivas, A., Marulanda, A., Ruiz-Lozano, J.M., Barea, J.M., Azcón, R. (2003). Influence of Bacillus sp. on physiological activities of two arbuscular mycorrhizal fungi and plant responses to PEG-induced drought stress. Mycorrhiza, 13, 249–256. DOI: 10.1007/s00572-003-0223-z
Walters, D.R., Paterson, L., Walsh, D.J., Havis, N.D. (2009). Priming for plant defense in barley provides benefits only under high disease pressure. Physiol. Mol. Plant Pathol., 73, 95–100. DOI: 10.1016/j.pmpp.2009.03.002
Wang, Q., Dodd, I.C., Belimov, A.A., Fan-Jiang, A.D. (2016). Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase growth and photosynthesis of pea plants under salt stress by limiting Na+ accumulation. Funct. Plant Biol., 43, 161–172. DOI: 10.1071/FP15200
Wu, S.J., Ding, L., Zhu, J.K. (1996). SOS1, a genetic locus essential for salt tolerance and potassium acquition. Plant Cell, 8, 617–627. DOI: 10.1105/tpc.8.4.617
Yamasaki, S., Dillenburg, L.R. (1999). Measurements of leaf relatıve water content in Araucaria angustifolia. Rev. Bras. Fisiol. Veg., 11, 69–75.
Yang, J., Kloepper, J.W., Ryu, C.M. (2008). Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci., 14, 1–4. DOI: 10.1016/j.tplants.2008.10.004
Yeole, R.D., Dube, H.C. (1997). Increased plant growth and yield through seed bacterization. Ind. Phytopathol., 50, 316–319.
Yıldız, S., Balkaya, A. (2016). The hypocotyls traits of salt tolerant winter squash and pumpkin rootstocks and the determination of grafting compatibility with cucumber. YYU J. Agric. Sci., 26, 538–546.
Yoshida, K. (2002). Plant biotechnology: Genetic engineering to enhance plant salt tolerance. J. Biosci. Bioeng., 94, 585–590. DOI: 10.1016/S1389-1723(02)80199-2
The Institute of Natural & Applied Sciences, Van Yuzuncu Yil University 65080 Van, Turkey https://orcid.org/0000-0002-0769-9171
Agricultural Biotechnology Department, Agriculture Faculty, Van Yuzuncu Yil University 65080 Van, Turkey https://orcid.org/0000-0003-1208-032X
Plant Protection Department, Agriculture Faculty, Van Yuzuncu Yil University 65080 Van, Turkey https://orcid.org/0000-0002-1526-6093
Baskale Vocational School, Van Yuzuncu Yil University, 65080 Van, Turkey https://orcid.org/0000-0002-0563-1130
License
Articles are made available under the conditions CC BY 4.0 (until 2020 under the conditions CC BY-NC-ND 4.0).
Submission of the paper implies that it has not been published previously, that it is not under consideration for publication elsewhere.
The author signs a statement of the originality of the work, the contribution of individuals, and source of funding.
