Document Type : Original Article
Authors
1 Department of Horticultural Science, Faculty of Agriculture, Urmia University, Iran
2 Department of Plant Production and Genetic, Faculty of Agriculture, Urmia University, Iran
3 Department of Soil Science, Faculty of Agriculture, Urmia University, Iran
4 Research Department of Chromatography, Iranian Academic Center for Education, Culture and Research (ACECR), Urmia, Iran
Abstract
To evaluate the effect of Piriformospora indica and Pseudomonas fluorescens inoculation on some growth and physiological parameters and nutrient acquisition of sage (Salvia officinalis) under salt stress conditions, a pot experiment was conducted in factorial based on randomized complete blocks design with three replications. The treatments included inoculation with microorganisms at three levels (non-inoculation and inoculation with P. indica and P. fluorescens) and salinity stress at four levels (0, 25, 50 and 100 mM of NaCl). The results showed that salinity stress and inoculation with microorganisms had significant effect on the measured parameters, so that by increasing salinity concentration, percentage of root colonization by P. indica,growth paramaters, leaf relative water content (RWC), chlorophyll index (SPAD), essential oil conten and yield, N, P and K content and K/Na ratio decreased while Na and Cl content increased. The amounts of all evaluated parameters in fungi and rhizobacteria inoculation were more than non-inoculation treatments except for Na and Cl content. The highest and lowest of dry herb yield (29.61 and 13.51 g pot-1), RWC (82.45 and 54.83%), chlorophyll content (35.36 and 26.1), essential oil content (2.02 and 1.37%), essential oil yield (0.049 and 0.017 ml plant-1) and P content (0.41 and 0.10%) were observed in non-stress conditions+ P. indica inoculated plants and 100 mM salinity+ non-inoculated plants, respectively. Overall, the findings of this study showed that plant growth-promoting microorganisms inoculation can ameliorate the adverse effects of salinity stress on growth, yield and essential oil production in sage by maintaining chlorophyll content and improving water and nutrient uptake.
Keywords
Ashraf M. 2002. Salt tolerance of cotton: some new advances. Critical Reviews in Plant Sciences, 21: 1-30.
Ashraf M., and Akhtar N. 2004. Influence of salt stress on growth, ion accumulation and seed oil content in sweet fennel. Biologia Plantarum, 48(3): 461-464.
Ashraf M., Hasnain S., Berge O., and Mahmood T. 2004. Inoculating wheat seedling with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biology and Fertility of Soils, 40(3):157-162.
Aziz E.E., Al-Amier H., and Craker L.E. 2008. Influence of salt stress on growth and essential oil production in peppermint, pennyroyal, and apple mint. Journal of Herbs, Spices and Medicinal Plants, 14: 77-87.
Baltruschat H., Fodor J., Harrach B.D., Niemczyk E., Barna B., Gullner G., Janeczko A., Kogel K.H., Schäfer P., Schwarczinger I., Zuccaro A., and Skoczowski A. 2008. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist, 180: 501-510.
Bano A., Fatima M. 2009. Salt tolerance in Zea mays (L.) following inoculation with Rhizobium and Pseudomonas. Biology and Fertility of Soils, 45(4): 405-413.
Barin M., Rasouli-Sadaghiani R.H., Ashrafi-Saeidlou, S., and Shakouri F. 2019. Effects of salinity and microbial inoculation on the yield and phosphorous efficiency indicators of corn. Applied Soil Research, 7(1): 148-165. (In Persian)
Bazyar M., Bandehagh A., and Farajzadeh D. 2017. Effect of inoculation of Pseudomonas fluorescens FY32 bacteria to reduce the effects of salinity on canola (Brassica napus L.). Journal of Crop Production, 9(4): 201-220.
Ben Taarit M., Msaada K., Hosni K., Hammami M., Kchouk M.E., and Marzouk B. 2009. Plant growth, essential oil yield and composition of sage (Salvia officinalis L.) fruits cultivated under salt stress conditions. Industrial Crops and Products, 30: 333-337.
Bharti N., Barnawal D., Awasthi A., Yadav A., and Kalra A. 2014. Plant growth promoting rhizobacteria alleviate salinity induced negative effects on growth, oil content and physiological status in Mentha arvensis. Acta Physiologiae Plantarum, 36: 45-60.
Canbolat M.Y., Bilen S., Çakmakçı R., Şahin F., and Aydin A. 2006. Effect of plant growth promoting bacteria and soil compaction on barley seedling growth, nutrient uptake, soil properties and rhizosphere microflora. Biology and Fertility of Soils, 42(4):350-357.
Chrysargyris A., Michailidi E., and Tzortzakis N. 2018. Physiological and biochemical responses of Lavandula angustifolia to salinity under mineral foliar application. Frontiers in Plant Science, 489: 1-23.
Coban O., and Baydar N.G. 2016. Brassinosteroid effects on some physical and biochemical properties and secondary metabolite accumulation in peppermint (Mentha piperita L.) under salt stress. Industrial Crops and Products, 86: 251-258.
Cotteni A. 1980. Methods of plant analysis. In: Westerman R.L. (Ed.), Soil and Plant Testing. FAO Soil Bulletin, pp. 64-100.
Dehghani Bidgoli R., Azarnezhad N., Akhbari M., and Ghorbani M. 2019. Salinity stress and PGPR effects on essential oil changes in Rosmarinus officinalis L. Agriculture and Food Security, 8: 1-7.
Egamberdieva D., Jabborova D., and Hashem A. 2015. Pseudomonas induces salinity tolerance in cotton (Gossypium hirsutum) and resistance to Fusarium root rot through the modulation of indole-3-acetic acid. Saudi Journal of Biological Sciences, 22: 773-779.
El-Keltawi N.E., and Croteau R., 1987. Salinity depression of growth and essential oil formation in spearmint and marjoram and its reversal by foliar applied cytokinin. Phytochemistry, 26: 1333-1334.
Emami Bistgani Z., Hashemi M., DaCosta M., Craker L., Maggi F., and Morshedloo M.R. 2019. Effect of salinity stress on the physiological characteristics, phenolic compounds and antioxidant activity of Thymus vulgaris L. and Thymus daenensis Celak. Industrial Crops and Products, 135: 311–320.
Emami A. 1996. Plant Analysis Methods. No. 982. Vol. 1. Soil and Water Research Institute Publication, Tehran. (In Persian)
Evelin H., Kapoor R., and Giri B. 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: A review. Annals of Botany, 104(7): 1263-1280.
Evelin H., Giri B., and Kapoor R. 2013. Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza, 23: 71-86.
Ghorbani A., Razavi S.M., Omran V.O.G., and Pirdashti H. 2018. Piriformospora indica alleviates salinity by boosting redox poise and antioxidative potential of tomato. Russian Journal of Plant Physiology, 65(6):898-907.
Ghorbanpour M., Hosseini N., Khodae Motlagh M., and Solgi M. 2014. The effects of inoculation with Pseudomonads rhizobacteria on growth, quantity and quality of essential oils in Sage (Salvia officinalis L.) plant. Journal of Medicinal Plants, 13(52): 89-100. (In Persian)
Hammer E.C., Nasr H., Pallon J., Olsson P.A., and Wallander H. 2011. Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza, 21: 117-129.
Hasnain S., and Sabri A.N. 1996. Growth stimulation of Triticum aestivum seedlings under Cr-stress by nonrhizospheric Pseudomonas strains. In: Abstract book of 7th International Symposium on Nitrogen Fixation with Non-Legumes. Faisalabad, Pakistan, pp- 36.
Hassanvanda H., Rezaei Nejada A., Fanourakisb D. 2019. Morphological and physiological components mediating the silicon-induced enhancement of geranium essential oil yield under saline conditions. Industrial Crops and Products, 134: 19-25.
Heidari Sharif Abad H. 2011. Plants and salinity. Research Institute of Forests and Rangelands Publications, Tehran, 199 p. (In Persian)
Isayenkov S.V. 2012. Physiological and molecular aspects of salt stress in plants. Cytology and Genetics, 46(5): 302-318.
Jindal V., Atwal A., and Singh R. 1993. Effect of Vesicular-arbuscular mycorrhizae on metabolism of moong plant under NaCl salinity. Plant Physiology, 31: 475-481.
Jogawat A., Saha S., Bakshi M., Dayaman V., Kumar M., Dua M., Varma A., Oelmüller R., Tuteja N., and Johri A.K. 2013. Piriformospora indica rescues growth diminution of rice seedlings during high salt stress. Plant Signaling and Behavior, 8(10): e26891.
Johnson J.M., and Ulrich A. 1975. Analytical methods for use in plant analysis. Bulletin 766. Berkeley: University of California, Agricultural Experiment Station, pp. 26-78.
Kadian N., Yadav K., Badda N., and Aggarwal A. 2013. AM fungi ameliorates growth, yield and nutrient uptake in Cicer arietinum L. under salt stress. Russian Agricultural Sciences, 39: 321-329.
Käfer E. 1977. Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Advanced Genetics, 19:33-131.
Kasotia A., Varma A., and Choudhary D.K. 2015. Pseudomonas-mediated mitigation of salt stress and growth promotion in Glycine max. Agricultural Research, 4(1): 31-41.
Khademian R., Asghari B., Sedaghati B., and Yaghoubian Y. 2019. Plant beneficial rhizospheric microorganisms (PBRMs) mitigate deleterious effects of salinity in sesame (Sesamum indicum L.): Physio-biochemical properties, fatty acids composition and secondary metabolites content. Industrial Crops and Products, 136: 129-139.
Khalvandi M., Amerian M., Pirdashti H., Baradaran M., and Golami A. 2017a. Piriformospora indica symbiotic effect on the quantity and quality of essential oils and some physiological parameters of peppermint (Mentha piperita) under salt stress. Journal of Plant Process and Function, 6(21): 169-184. (In Persian)
Khalvandi M., Amerian M., Pirdashti H., Baradaran M., and Golami A. 2017b. Effects of Piriformospora indica fungi symbiotic on the quantity of essential oil and some physiological parameters of peppermint in saline conditions. Iranian Journal of Plant Biology, 32:1-19. (In Persian)
Khalvandi M., Amerian M., Pirdashti H., Keramati S., and Hosseini J. 2019. Essential oil of peppermint in symbiotic relationship with Piriformospora indica and methyl jasmonate application under saline condition. Industrial Crops and Products, 127: 195-202.
Khorsandi O., Hassani A., Sefidkon F., Shirzad H., and Khorsandi A.R. 2010. Effect of salinity (NaCl) on growth, yield, essential oil content and composition of Agastache foeniculum Kuntz. Iranian Journal of Medicinal and Aromatic Plant, 26(3): 438-451. (In Persian)
Kohler J., Hernández J.A., Fuensanta Caravaca F., and Roldan A. 2009. Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environmental and Experimental Botany, 65: 245–252.
Kulak M., Gul F., and Sekeroglu N. 2020. Changes in growth parameter and essential oil composition of sage (Salvia officinalis L.) leaves in response to various salt stresses. Industrial Crops and Products, 145: 112078.
McMillen B.G., Juniper S., and Abbott L.K. 1998. Inhibition of hyphal growth of a Vesicular arbuscular mycorrhizal fungus in soil containing sodium chloride limits the spread of infection from spores. Soil Biology and Biochemistry, 30(13): 1639-1646.
Meena K.K., Mesapogu S., Kumar M., Yandigeri M.S., Singh G., and Saxena A.K. 2010. Co-inoculation of the endophytic fungus Piriformospora indica with the phosphate-solubilising bacterium Pseudomonas striata affects population dynamics and plant growth in chickpea. Biology and Fertility of Soils, 46(2): 169-174.
Meena V.S., Meena S.K., Verma J.P., Kumar A., Aeron A., Mishra P.K., Bisht J.K., Pattanayak A., Naveed M., and Dotaniya M.L. 2017. Plant beneficial rhizospheric microorganism (PBRM) strategies to improve nutrients use efficiency: a review. Ecological Engineering, 107: 8–32.
Mohamed H.I., and Gomma E.Z. 2012. Effect of plant growth promoting Bacillus subtilis and Pseudomonas fluorescens on growth and pigment composition of radish plants (Raphanus sativus) under NaCl stress. Photosynthetica, 50(2): 263-272.
Mulvaney R.L. 1996. Nitrogen-inorganic forms. In: Sparks D.L. (Ed.). Methods of Soil Analysis-Part 3. Chemical Methods—SSSA Book Series No. 5. Soil Science Society of America and American Society of Agronomy, Madison, pp. 1123–1184.
Munns R. 2002. Comparative physiology of salt and water stress. Plant Cell Environment, 25: 239-250.
Nadeem S.M., Zahir Z.A., Naveed M., and Arshad M. 2009. Rhizobacteria containing ACC-deaminase confer salt tolerance in maize grown on salt-affected fields. Canadian Journal of Microbiology, 55(11): 1302-1309.
Parida A.K., Das A.B., and Mittra B. 2004. Effects of salt on growth, ion accumulation, photosynthesis and leaf anatomy of the mangrove. Trees, 18(2): 167-174.
Parida A.K., and Das A.B. 2005. Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety, 60: 324-349.
Philips J., and Hayman D. 1970. Improved procedures for cleaning roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society, 55(1): 158-161.
Raal A., Orav A., and Arak E. 2007. Composition of the essential oil of Salvia officinalis L. from various European countries. Natural Product Research, 21: 406-411.
Rajkumar M., Bruno L.B., and Banu J.R. 2017. Alleviation of environmental stress in plants: the role of beneficial Pseudomonas spp. Critical Reviews in Environmental Science and Technology, 47(6): 372-407.
Rasouli-Sadaghiani R.H., Barin M., Ashrafi-Saeidlou, S., and Shakouri F. 2019. Effects of phosphate-solubilizing microorganisms and mycorrhizal fungi on the growth parameters of corn (Zea Mays L.) under salinity condition. Applied Soil Research, 7(3): 25-39. (In Persian)
Reyes-Castillo A., Gerding M., Oyarzúa P., Zagal E., Gerding J., and Fischer S. 2017. Plant growth-promoting rhizobacteria able to improve NPK availability: selection, identification and effects on tomato growth. Chilean Journal of Agricultural Research, 79(3): 473-485.
Saberi-Riseh R., Fathi F., and Moradzadeh-Eskandari M. 2020. Effect of some Pseudomonas fluorescens and Bacillus subtilis strains on osmolytes and antioxidants of cucumber under salinity stress. Journal of Crop Protection, 9(1): 1-16.
Santos C.V. 2004. Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Scientia Horticulturae, 103: 93-99.
Selmar, D. 2008. Potential of salt and drought stress to increase pharmaceutical significant secondary compounds in plants. Agriculture and Forest Research, 58: 139-144.
Serrano R., and Rodriguez-Navarr A. 2001. Ion homeostasis during salt stress in plants. Current Opinion in Cell Biology,13: 399-404.
Siddiqui M.N., Mohammad F., Khan, M.M.A., and Al-Whaibi M.H. 2012. Cumulative effect of nitrogen and sulphur on Brassica juncea L. genotypes under NaCl stress. Protoplasma, 249: 139-153.
Sirrenberg A., Göbel C., Grond S., Czempinski N., Ratzinger A., Karlovsky P., Santos P., Feussner I., and Pawlowski K. 2007. Piriformospora indica affects plant growth by auxin production. Physiologia Plantarum, 131: 581–589.
Tabatabaei S.J. 2006. Effect of salinity and N on the growth photosynthesis and N status of oliv (Olea europaea L.) trees. Scientia Horticulturae, 108(4): 432-438.
Turner N.C. 1981. Techniques and experimental approaches for the measurement of plant water status. Plant and Soil, 58: 339-366.
Weiss M., Selosse M.A., Rexer K.H., Urban A., and Oberwinkler F. 2004. Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycological Research, 108: 1003-1010.
Yang J.W., Kloepper J.W., and Ryu C.M. 2008. Rhizosphere bacteria help plants tolerate abiotic stress. Trends in Plant Science, 14: 1-4.
Yasar F., Ellialtioglu S., and Yildiz K. 2008. Effect of salt stress on antioxidant defense systems, lipid peroxidation, and chlorophyll content in green bean. Russian Journal of Plant Physiology, 55(6): 869-873.
Yu Y., Xu T., Li X., Tang J., Ma D., Li Z., and Sun J. 2016. NaCl-induced changes of ion homeostasis and nitrogen metabolism in two sweet potato (Ipomoea batatas L.) cultivars exhibit different salt tolerance at adventitious root stage. Environmental and Experimental Botany, 129: 23-36.
Yun P., Xu L., Wang S., Shabala L., Shabala S., and Zhang W.Y. 2018. Piriformospora indica improves salinity stress tolerance in Zea mays L. plants by regulating Na+ and K+ loading in root and allocating K+ in shoot. Plant Growth Regulation, 86(2): 323-331.
Zarea M.J., Hajinia S., Karimi N., Mohammadi G.E., Rejali F., and Varma, A. 2012. Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biology and Biochemistry, 45: 139-146.
Zhu J.K. 2001. Plant salt tolerance. Trends in Plant Science, 6(2): 66-71.
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