Increased tolerance of Mexican lime (Citrus aurantifolia Swingle) seedlings to salinity stress when inoculated with endophytes spergillus nigerA and Bacillus aquimaris extracted from seaweed

Document Type : Research Paper

Authors

1 Ph.D. in Biotechnology and Molecular Genetics of Horticultural Products, Hormozgan University, Bandar Abbas, Iran

2 Associate Professor in Horticultural Science Department, Agriculture and Natural Resources College, University of Hormozgan, Bandar Abbas, Iran

3 Assistant Professor in Plant Protection Research Department, Hormozgan Agricultural and Natural Resources Research and Education Center, Agricultural Research, Education and Extension Organization (AREEO), Bandar Abbas, Iran

4 Assistant Professor in Hormozgan Agricultural and Natural Resources Research and Education Center, Agricultural Research, Education and Extension Organization (AREEO), Bandar Abbas, Iran

10.22124/japb.2022.20908.1444

Abstract

Endophytes play an important role in protecting plants. In this study, endophytic combination of Aspergillus niger and Bacillus aquimaris OD14 was used to improve tolerance of Mexican lime seedlings to salinity stress. Three months after inoculation, salinity stress of 0, 2000, 4000 and 6000 μs/cm was applied. After 8 weeks, morphological, biochemical and elements adsorption traits of seedlings were evaluated. The experiment was carried out as factorial in a completely randomized design with three replications. The results showed that in 6000 μs/cm water salinity, endophytic compound increased stem length (103.64%), trunk diameter (103.04%), number of leaves (444.41%) and root length and width (232.02% and 41.63% respectively). Endophyte increased 76.29% of SPAD chlorophyll content compared to control. Also, the uptake of root potassium (34.95%) and shoot calcium (115.15%) increased and the uptake of sodium elements was decreased (29.49%) compared to control. Endophytic combination could significantly reduce ion leakage (65.57%) and increase proline content (69.3%) in inoculated seedlings compared to control. In general, marine endophytes can be used as a suitable option to increase plant tolerance to salinity.

Keywords

References

Aboutalebi A. and Hassanzadeh H. 2016. Effect of humic acid on some vegetative traits and ion concentrations of Mexican lime (Citrus aurantifolia Swingle) seedlings under salt stress. International Journal of Horticultural Science and Technology, 3(2): 255–264.
Ali A., Shahzad R., Khan A.L., Halo B.A., Al-Yahyai R., Al-Harrasi A., Al-Rawahi A. and Lee I.J. 2017. Endophytic bacterial diversity of Avicennia marina helps to confer resistance against salinity stress in Solanum lycopersicum. Journal of Plant Interactions, 12(1): 312–322.
Al-Yassin A. 2005. Adverse effects of salinity on Citrus. International Journal of Agriculture and Biology, 7(4): 668–680.
Arnold A.E. and Lutzoni F. 2007. Diversity and host range of foliar fungal endophytes: Are tropical leaves biodiversity hotspots? Ecology, 88(3): 541–549.
Ashraf M. and McNeilly T. 2004. Salinity tolerance in Brassica oilseeds. Critical Reviews in Plant Sciences, 23(2): 157–174.
Auge R.M., Stodola A.J., Tims J.E. and Saxton A.M. 2001. Moisture retention properties of a mycorrhizal soil. Plant and Soil, 230(1): 87–97.
Bandari Z., Mozamian E. and Azarpira N. 2016. Investigating the cytotoxic effects of Persian Gulf marine Actinomycetes protease on blood cancer cell line. Basic and Clinical Cancer Research, 8(4): 3–14.
Bates L.S., Waldren R.P. and Teare I.D. 1973. Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1): 205–207.
Bhadury P., Mohammad B.T. and Wright P.C. 2006. The current status of natural products from marine fungi and their potential as anti-infective agents. Journal of Industrial Microbiology and Biotechnology, 33(5): 325–337.
Bhattacharyya P.N.J. 2012. Plantgrowth-promotingrhizobacteria (PGPR): Emergencein agriculture. World Journal of Microbiology Biotechnology, 28: 1327–1350.
Bibi F., Yasir M., Song G.C., Lee S.Y. and Chung Y.R. 2012. Diversity and characterization of endophytic bacteria associated with tidal flat plants and their antagonistic effects on oomycetous plant pathogens. Plant Pathology Journal, 28(1): 20–31.
Bu N., Li X., Li Y., Ma C., Ma L. and Zhang C. 2012. Effects of Na2CO3 stress on photosynthesis and antioxidative enzymes in endophyte infected and non-infected rice. Ecotoxicology and Environmental Safety, 78: 35–40.
Chapman H.D. and Pratt P.P. 1961. Methods of Analysis for Soils, Plants and Waters. University of California Publications, USA. 309P.
Choudhary D.K., Kasotia A., Jain S., Vaishnav A., Kumari S., Sharma K.P. and Varma A. 2016. Bacterial-mediated tolerance and resistance to plants under abiotic and biotic stresses. Journal of Plant Growth Regulation, 35(1): 276–300.
Dhindsa R.S., Plumb-Dhindsa P.A.M.E.L.A. and Thorpe T.A. 1981. Leaf senescence: Correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. Journal of Experimental botany, 32(1): 93–101.
Dodd I.C. and Perez-Alfocea F. 2012. Microbial amelioration of crop salinity stress. Journal of Experimental Botany, 63(9): 3415–3428.
Fricke W. and Peters W.S. 2002. The biophysics of leaf growth in salt-stressed barley. A study at the cell level. Plant Physiology, 129(1): 374–388.
Garcia-Legaz M.F., Lopez-Gomez E., Beneyto J.M., Navarro A. and Sanchez-Blanco M.J. 2008. Physiological behavior of loquat and anger rootstocks in relation to salinity and calcium addition. Journal of Plant physiology, 165(10): 1049–1060.
Garcia-Sanchez F., Jifon J.L., Carvajal M. and Syvertsen J.P. 2002. Gas exchange, chlorophyll and nutrient contents in relation to Na+ and Cl− accumulation in ‘Sunburst’ mandarin grafted on different rootstocks. Plant Science, 162(5): 705–712.
Gimeno V., Syvertsen J.P., Nieves M., Simon I., Martinez V. and Garcia-Sanchez F. 2009. Additional nitrogen fertilization affects salt tolerance of lemon trees on different rootstocks. Scientia Horticulturae, 121(3): 298–305.
Hamilton C.E. and Bauerle T.L. 2012. A new currency for mutualism? Fungal endophytes alter antioxidant activity in hosts responding to drought. Fungal Diversity, 54(1): 39–49.
Hardoim P.R., Van Overbeek L.S., Berg G., Pirttila A.M., Compant S., Campisano A., Doring M. and Sessitsch A. 2015. The hidden world within plants: Ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews, 79(3): 293–320.
Hepaksoy S. 2000. Effect of salinity on Citrus. Anadolu Journal of Aegean Agricultural Research Institute, 10(1): 52–72.
Hindersah R., Rahmadina I., Harryanto R., Suryatmana P. and Arifin M. 2021. Bacillus and Azotobacter counts in solid biofertilizer with different concentration of zeolite and liquid inoculant. The 2nd International Conference on Agriculture and Bio-industry. IOP Conference Series, Indonesia: Earth and Environmental Science, 667: 1–6.
Jin N., Liu S.M., Peng H., Huang W.K., Kong L.A., Wu Y.H., Chen Y.P., Ge F.Y., Heng Jian H. and De-Liang Peng D.L. 2019. Isolation and characterization of Aspergillus niger NBC001 underlying suppression against Heterodera glycines. Scientific Reports, 9: 1–13 (591).
Kalyani P. and Hemalatha K.P.J. 2016. Review paper-marine microbial bioactive compounds. International Journal of Engineering Sciences and Research Technology, 5(11): 124–133.
Kaya M.D., Okçu G., Atak M., Cikili Y., Kolsarici O. 2006. Seed treatments to overcome salt and drought stress during germination in sunflower (Helianthus annuus L.). European journal of Agronomy, 24(4): 291–295.
Kishor P.K., Sangam S., Amrutha R.N., Laxmi P.S., Naidu K.R., Rao K.S., Rao S., Reddy K.J., Theriappan P. and Sreenivasulu N. 2005. Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance. Current Science, 88(3): 424–438.
Ling Q., Huang W. and Jarvis P. 2011. Use of a SPAD-502 meter to measure leaf chlorophyll concentration in Arabidopsis thaliana. Photosynthesis Research, 107(2): 209–214.
Mahmoudi M. and Zoghalchali H.B. 2015. The effects of humic substances on some physiological properties of Citrus sinensis cv. Thomson navel under lime condition. International Research Journal of Applied and Basic Sciences, 9(1): 132–135.
Meggio F., Prinsi B., Negri A.S., Simone Di Lorenzo G., Lucchini G., Pitacco A., Failla O., Scienza A., Cocucci M. and Espen L. 2014. Biochemical and physiological responses of two grapevine rootstock genotypes to drought and salt treatments. Australian Journal of Grape and Wine Research, 20(2): 310–323.
Mei C., Lara-Chavez A., Lowman S. and Flinn B. 2014. The use of endophytes and mycorrhizae in switch grass biomass production. P: 67–108. In: Luo H. and Wu Y. (Eds.). Compendium of Bioenergy Plants. CRC Press, USA.
Mishra S., Singh A., Keswani C., Saxena A., Sarma B.K. and Singh H.B. 2015. Harnessing plant-microbe interactions for enhanced protection against phytopathogens. P: 111–125. In: Arora N.K. (Ed.). Plant Microbes Symbiosis: Applied Facets. Springer, India.
Moya J.L., Primo‐Millo E. and Talon M. 1999. Morphological factors determining salt tolerance in Citrus seedlings: The shoot to root ratio modulates passive root uptake of chloride ions and their accumulation in leaves. Plant, Cell and Environment, 22(11): 1425–1433.
Mukherjee K. and Sen B. 1998. Biological control of fusarium wilt of muskmelon by formulations of Aspergillus niger. Israel Journal of Plant Sciences, 46(1): 67–72.
Munns R. and Tester M. 2008. Mechanisms of salinity tolerance. Annual Review Plant Biology, 59: 651–681.
Munns R., Wallace P.A., Teakle N.L. and Colmer T.D. 2010. Measuring soluble ion concentrations (Na+, K+, Cl−) in salt-treated plants. P: 371–382. In: Sunkar R. (Ed.). Plant Stress Tolerance. Humana Press, USA.
Nenkep V.N., Yun K., Li Y., Choi H.D., Kang J.S. and Son B.W. 2010. New production of haloquinones, bromochlorogentisylquinones A and B, by a halide salt from a marine isolate of the fungus Phoma herbarum. The Journal of Antibiotics, 63(4): 199–201.
Newman D.J. and Hill R.T. 2006. New drugs from marine microbes: The tide is turning. Journal of Industrial Microbiology and Biotechnology, 33(7): 539–544.
Nishihara E., Kondo K., Parvez M.M., Takahashi K., Watanabe K. and Tanaka K. 2003. Role of 5-aminolevulinic acid (ALA) on active oxygen-scavenging system in NaCl-treated spinach (Spinacia oleracea). Journal of Plant Physiology, 160(9): 1085–1091.
Page M.J. and Di Cera E. 2006. Role of Na+ and K+ in enzyme function. Physiological Reviews, 86(4): 1049–1092.
Pal S., Singh H.B., Farooqui A. and Rakshit A. 2015. Fungal biofertilizers in Indian agriculture: Perception, demand and promotion. Journal of Eco-Friendly Agriculture, 10(2): 101–113.
Qiao J.Q., Wu H.J., Huo R., Gao X.W. and Borriss R. 2014.  Stimulation of plant growth and biocontrol by Bacillus amyloliquefaciens subsp. plantarum FZB42 engineered for improved action. Chemical and Biological Technologies in Agriculture, 1: 1–14 (12).
Radhakrishnan R., Hashem A. and Abd Allah E.F. 2017. Bacillus: A biological tool for crop improvement through bio-molecular changes in adverse environments. Frontiers in Physiology, 8: 1–14 (667).
Redman R.S., Kim Y.O., Woodward C.J., Greer C., Espino L., Doty S.L. and Rodriguez R.J. 2011. Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: A strategy for mitigating impacts of climate change. PLOS One, 6(7): 1–10 (e14823).
Rivero R.M., Shulaev V. and Blumwald E. 2009. Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiology, 150(3): 1530–1540.
Saravanakumar D. and Samiyappan R. 2007. ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. Journal of Applied Microbiology, 102(5): 1283–1292.
Shahid M.A., Pervez M.A., Balal R.M., Mattson N.S., Rashid A., Ahma R., Ayyub C.M. and Abbas T. 2011. Brassinosteroid (24-epibrassinolide) enhances growth and alleviates the deleterious effects induced by salt stress in pea (Pisum sativum L.). Australian Journal of Crop Science, 5(5): 500–510.
Sun B., Gu L., Bao L., Zhang S., Wei Y., Bai Z., Zhuang G. and Zhuang X. 2020. Application of biofertilizer containing Bacillus subtilis reduced the nitrogen loss in agricultural soil. Soil Biology and Biochemistry, 148: 1–47 (107911).
Toth S.Z., Schansker G., Kissimon J., Kovacs L. and Strasser R.J. 2005. Biophysical studies of photosystem II-related recovery processes after a heat pulse in barley seedlings (Hordeum vulgare L.). Journal of Plant Physiology, 162(2): 181–194.
Vaishnav A., Varma A., Tuteja N. and Choudhary D.K. 2017. Characterization of bacterial volatiles and their impact on plant health under abiotic stress. P: 15–24. In: Choudhary D., Sharma A., Agarwal P., Varma A. and Tuteja N. (Eds.). Volatiles and Food Security. Springer, Singapore.
Victor K., Okoth S., De Boevre M. and De Saeger S. 2019. Biocontrol of Aspergillus and Fusarium mycotoxins in Africa. Benefits and Limitations of Toxins, 11(2): 1–9 (109).
Waqas M., Khan A.L., Hamayun M., Shahzad R., Kang S.M., Kim J.G. and Lee I.J. 2015. Endophytic fungi promote plant growth and mitigate the adverse effects of stem rot: An example of Penicillium citrinum and Aspergillus terreus. Journal of Plant Interactions, 10(1): 280–287.
Whitlow T.H., Bassuk N.L., Ranney T.G. and Reichert D.L. 1992. An improved method for using electrolyte leakage to assess membrane competence in plant tissues. Plant Physiology, 98(1): 198–205.
Yokoi S., Bressan R.A. and Hasegawa P.M. 2002. Salt stress tolerance of plants. JIRCAS Working Report, 23(1): 25–33.
Zekri M. and Parsons L.R. 1990. Calcium influences growth and leaf mineral concentration of Citrus under saline conditions. Horticulture Science, 25(7): 784–786.
Aquatic Physiology and Biotechnology
Volume 10, Issue 3
January 2023
Pages 119-147

Files

Share

How to cite

Statistics