Abstract
Understanding plant microbes’ intimate relationship and search for beneficial microbes is a sustainable alternative to improve plant growth and yield under a wide range of biotic and abiotic stress conditions. More than 20% of the total global agricultural land is affected by salinity. High salinity challenges crop plants by affecting several metabolic pathways and decreasing plant growth and yield. Unlike chemical fertilizers and pesticides, endophytic microbes offer an eco-friendly approach to increasing crop yield via various metabolites during salinity stress. The objective of this study was to isolate and characterize endophytic halotolerant bacterial isolates from haloalkaliphytes, investigate their plant growth-promoting (PGP) properties and tolerance for various stress conditions. Sporobolus specatus (Vahr) Kunth and Cyperus laevigatus L. grass samples were collected from the shores of two Ethiopian soda lakes (Lakes Abijata, and Chitu, respectively). A total of 167 halotolerant endophytic bacterial isolates, that clustered into 21 ARDRA (Amplified ribosomal DNA restriction analysis) groups, affiliated to members of 11 bacterial genera, namely Halomonas, Agrobacterium, Exiguobacterium, Jonesia, Stenotrophomonas, Pseudomonas, Alishewanella, Kosakonia, Bacillus, Paracoccus and Pannonibacter, were identified based on 16S rRNA sequencing. Most of the strains were able to produce IAA (indole-3-acetic acid) and hydrogen cyanide, grow on a nitrogen-free medium and solubilize phosphate. In vitro tolerance tests reveal that isolates were tolerant to: 5.0–15% NaCl, up to 40% PEG 6000, temperatures up to 50 °C, and pH 5–11. These characteristics of the isolates indicate their potential PGP application under various plant stress conditions.
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Data availability
“The datasets generated during and/or analyzed during the current study are submitted as electronic figures and available from the corresponding author”. Molecular sequence data are available in NCBI (ACC. MW418101–MW418121).
References
Ali SZ, Sandhya V, Rao LV (2014) Isolation and characterization of drought-tolerant ACC deaminase and exopolysaccharide-producing fluorescent Pseudomonas sp. Ann Microbiol 64:493–502. https://doi.org/10.1007/s13213-013-0680-3
Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Atlas RM (2004) Handbook of microbiological media. CRC Press, Boca Raton
Bashan Y (2014) Bacteria / Plant growth-promotion. In: Hillel D (ed) Encyclopedia of soils in the environment. Elsevier Ltd, Oxford, UK, pp 103–115
Behera P, Mahapatra M, Seuylemezian A et al (2018) Taxonomic description and draft genome of Pseudomonas sediminis sp. nov., isolated from the rhizospheric sediment of Phragmites karka. J Microbiol 56:458–466. https://doi.org/10.1007/s12275-018-7549-x
Bodhankar S, Grover M, Hemanth S et al (2017) Maize seed endophytic bacteria: dominance of antagonistic, lytic enzyme-producing Bacillus spp. 3 Biotech 7:232. https://doi.org/10.1007/s13205-017-0860-0
Borsodi AK, Micsinai A, Rusznyák A et al (2005) Diversity of alkaliphilic and alkalitolerant bacteria cultivated from decomposing reed rhizomes in a Hungarian soda lake. Microb Ecol 50:9–18. https://doi.org/10.1007/s00248-004-0063-1
Brolezzi, M, Lincopan N, Ichiwaki, S, Ferrara F, Barbosa H (2015) Molecular characteristics of Enterobacteriaceae isolated from sugarcane and clinical samples. NCBI database. https://www.ncbi.nlm.nih.gov/nuccore/KR558702. Accessed 25 Jan 2022
Chen S, Xing J, Lan H (2012) Comparative effects of neutral salt and alkaline salt stress on seed germination, early seedling growth and physiological response of a halophyte species Chenopodium glaucum. Afr J Biotechnol 11:9572–9581. https://doi.org/10.5897/ajb12.320
Crapart S, Fardeau M-L, Cayol J-L et al (2007) Exiguobacterium profundum sp. nov., a moderately thermophilic, lactic acid-producing bacterium isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 57:287–292. https://doi.org/10.1099/ijs.0.64639-0
Das J, Sultana S, Rangappa K et al (2020) Endophyte bacteria alter physiological traits and promote growth of rice (Oryza sativa L.) in aluminium toxic and phosphorus deficient acid inceptisols. J Pure Appl Microbiol 14:627–639
Day AD, Ludeke KL (1993) Soil Alkalinity. In: Day AD et al (eds) Plant Nutrients in Desert Environments. Springer-Verlag, Berlin Heidelberg, pp 35–37. https://doi.org/10.1007/978-3-642-77652-6_9
Desgarennes D, Garrido E, Torres-Gomez MJ et al (2014) Diazotrophic potential among bacterial communities associated with wild and cultivated Agave species. FEMS Microbiol Ecol 90:844–857. https://doi.org/10.1111/1574-6941.12438
Dixit VK, Misra S, Mishra SK et al (2020) Characterization of plant growth-promoting alkalotolerant Alcaligenes and Bacillus strains for mitigating the alkaline stress in Zea mays Antonie Van Leeuwenhoek. Int J Gen Mol Microbiol 113:889–905. https://doi.org/10.1007/s10482-020-01399-1
Egamberdieva D, Wirth S, Bellingrath-Kimura SD et al (2019) Salt-tolerant plant growth promoting rhizobacteria for enhancing crop productivity of saline soils. Front Microbiol 10:1–18. https://doi.org/10.3389/fmicb.2019.02791
Ek-Ramos MJ, Gomez-Flores R, Orozco-Flores AA et al (2019) Bioactive products from plant-endophytic Gram-positive bacteria. Front Microbiol 10:1–12. https://doi.org/10.3389/fmicb.2019.00463
Enebe MC, Babalola OO (2018) The influence of plant growth-promoting rhizobacteria in plant tolerance to abiotic stress: a survival strategy. Appl Microbiol Biotechnol 102:7821–7835. https://doi.org/10.1007/s00253-018-9214-z
Enquahone S, van Marle G, Gessesse A, Simachew A (2020) Molecular identification and evaluation of the impact of red heat damage causing halophilic microbes on salted hide and skin. Int Biodeterior Biodegrad 150:104940. https://doi.org/10.1016/j.ibiod.2020.104940
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution (n y) 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Giovannoni S (1991) The polymerase chain reaction. John Wiley and Sons Ltd, West Sussex, UK
Gordon SA, Weber RP (1950) Colorimetric estimation of indole-3-acetic acid. Anal Biochem 72:134–138. https://doi.org/10.1016/0003-2697(76)90514-5
Granada CE, Passaglia LMP, de Souza EM, Sperotto RA (2018) Is phosphate solubilization the forgotten child of plant growth-promoting rhizobacteria? Front Microbiol 9:2054. https://doi.org/10.3389/fmicb.2018.02054
Gupta A, Bignoli J (2018) Cyperus laevigatus, smooth flatsedge. IUCN Red List Threat Species eT164060A65923957, 8235:1–8 https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T164060A65923957.en
Hall TA (1999) BioEdit software, version 5.0.9. North Carolina State University, Raleigh
Hirota K, Yamahira K, Nakajima K et al (2011) Pseudomonas toyotomiensis sp. nov., a psychrotolerant facultative alkaliphile that utilizes hydrocarbons. Int J Syst Evol Microbiol 61:1842–1848. https://doi.org/10.1099/ijs.0.024612-0
Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877. https://doi.org/10.1101/gr.9.9.868
Jensen BYHL (1948) Notes on the biology of Azotbacter. Proc Soc Appl Bacteriol 14:89–94. https://doi.org/10.1111/j.1365-2672.1951.tb01997.x
Jukes TH, Cantor CR (1969) Evolution of protein molecules. Mamm Protein Metab 3:21–132
Kandalepas D, Blum MJ, Van Bael SA (2015) Shifts in symbiotic endophyte communities of a foundational salt marsh grass following oil exposure from the deepwater horizon oil spill. PLoS One 10:1–18. https://doi.org/10.1371/journal.pone.0122378
Kandel SL, Joubert PM, Doty SL (2017) Bacterial endophyte colonization and distribution within plants. MDPI 5:77. https://doi.org/10.3390/microorganisms5040077
Kearl J, McNary C, Lowman JS et al (2019) Salt-tolerant halophyte rhizosphere bacteria stimulate growth of alfalfa in salty soil. Front Microbiol 10:1849. https://doi.org/10.3389/fmicb.2019.01849
Khan MA, Qaiser M (2006) Halophytes of Pakistan: characteristics, distribution and potential economic usages. Sabkha Ecosyst. https://doi.org/10.1007/978-1-4020-5072-5_11
Kim KK, Lee KC, Oh H-M, Lee J-S (2010) Halomonas stevensii sp. nov., Halomonas hamiltonii sp. nov. and Halomonas johnsoniae sp. nov., isolated from a renal care centre. Int J Syst Evol Microbiol 60:369–377. https://doi.org/10.1099/ijs.0.004424-0
Kipkemboi J (2016) Vascular plants in eastern Africa Rift Valley saline wetlands. Soda Lakes East Afr. https://doi.org/10.1007/978-3-319-28622-8_11
Kolekar YM, Pawar SP, Adav SS et al (2013) Alishewanella solinquinati sp. nov., isolated from soil contaminated with textile dyes. Curr Microbiol 67:454–459. https://doi.org/10.1007/s00284-013-0385-7
Kudoyarova GR, Melentiev AI, Martynenko EV et al (2014) Cytokinin producing bacteria stimulate amino acid deposition by wheat roots. Plant Physiol Biochem 83:285–291. https://doi.org/10.1016/j.plaphy.2014.08.015
Kulkarni S, Dhakar K, Joshi A (2019) Alkaliphiles: diversity and bioprospection. Microb Divers Genom Era. https://doi.org/10.1016/B978-0-12-814849-5.00015-0
Kulshreshtha NM, Kumar R, Begum Z et al (2013) Exiguobacterium alkaliphilum sp. nov. isolated from alkaline wastewater drained sludge of a beverage factory. Int J Syst Evol Microbiol 63:4374–4379. https://doi.org/10.1099/ijs.0.039123-0
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lanzen A, Simachew A, Gessesse A et al (2013) Surprising prokaryotic and eukaryotic diversity, community structure and biogeography of Ethiopian soda lakes. PLoS One 8:e72577. https://doi.org/10.1371/journal.pone.0072577
Lin L, Li Z, Hu C et al (2012) Plant growth-promoting nitrogen-fixing enterobacteria are in association with sugarcane plants growing in Guangxi, China. Microbes Environ 27:391–398. https://doi.org/10.1264/jsme2.ME11275
Lin P, Yan Z-F, Won K-H et al (2017) Paracoccus hibiscisoli sp. nov., isolated from the rhizosphere of Mugunghwa (Hibiscus syriacus). Int J Syst Evol Microbiol 67:2452–2458
Lorck H (1948) Production of hydrocyanic acid by bacteria. Physiol Plant 1:142–146. https://doi.org/10.1111/j.1399-3054.1948.tb07118.x
Maheshwari R, Bhutani N, Bhardwaj A, Suneja P (2019) Functional diversity of cultivable endophytes from Cicer arietinum and Pisum sativum: Bioprospecting their plant growth potential. Biocatal Agric Biotechnol 20:101229. https://doi.org/10.1016/j.bcab.2019.101229
Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940. https://doi.org/10.2135/cropsci2000.404923x
Manickam N, Ghosh A, Jain RK, Mayilraj S (2008) Description of a novel indole-oxidizing bacterium Pseudomonas indoloxydans sp. nov., isolated from a pesticide-contaminated site. Syst Appl Microbiol 31:101–107. https://doi.org/10.1016/j.syapm.2008.02.002
Marcum KB (2006) Use of saline and non-potable water in the turfgrass industry: constraints and developments. Agric Water Manag 80:132–146. https://doi.org/10.1016/j.agwat.2005.07.009
Martins RF, Davids W, Abu Al-Soud W et al (2001) Starch-hydrolyzing bacteria from Ethiopian soda lakes. Extremophiles 5:135–144. https://doi.org/10.1007/s007920100183
Marulanda A, Barea JM, Azcón R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM Fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Regul 28:115–124. https://doi.org/10.1007/s00344-009-9079-6
Meerak J, Yukphan P, Miyashita M et al (2008) Phylogeny of γ-polyglutamic acid-producing Bacillus strains isolated from a fermented locust bean product manufactured in West Africa. J Gen Appl Microbiol 54:159–166
Mehnaz S (2011) Plant growth-promoting bacteria associated with sugarcane. Bact Agrobiol Crop Ecosyst. https://doi.org/10.1007/978-3-642-18357-7_7
Misra S, Dixit VK, Mishra SK, Chauhan PS (2019) Demonstrating the potential of abiotic stress-tolerant Jeotgalicoccus huakuii NBRI 13E for plant growth promotion and salt stress amelioration. Ann Microbiol 69:419–434. https://doi.org/10.1007/s13213-018-1428-x
Moore E, Arnscheidt A, Krüger A et al (1999) Simplified protocols for the preparation of genomic DNA from bacterial cultures. In: Akkermans ADI (ed) Molecular microbial ecology manual. Kluwer Academic Press, pp 1–15
Muthukumar A, Udhayakumar R, Naveenkumar R (2017) Role of bacterial endophytes in plant disease control. In: Role of bacterial endophytes in plant disease control. pp 133–161
Muthukumarasamy R, Revathi G, Seshadri S, Lakshminarasimhan C (2002) Gluconacetobacter diazotrophicus (syn. Acetobacter diazotrophicus), a promising diazotrophic endophyte in tropics. Curr Sci 83:137–145
Olsen GJ, Matsuda H, Hagstrom R, Overbeek R (1994) fastDNAml: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Bioinformatics 10:41–48. https://doi.org/10.1093/bioinformatics/10.1.41
Otieno N, Lally RD, Kiwanuka S et al (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol 6:745. https://doi.org/10.3389/fmicb.2015.00745
Otten L, De Ruffray P (1996) Major differences between the rrnA operons of two strains of Agrobacterium vitis. Arch Microbiol 166:68–70. https://doi.org/10.1007/s002030050357
Øvreås L, Forney L, Daae FL, Torsvik V (1997) Distribution of bacterioplankton in meromictic lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63:3367–3373. https://doi.org/10.1128/aem.63.9.3367-3373.1997
Paul D, Nair S (2008) Stress adaptations in a plant growth promoting rhizobacterium (PGPR) with increasing salinity in the coastal agricultural soils. J Basic Microbiol 48:378–384. https://doi.org/10.1002/jobm.200700365
Peng G, Zhang W, Luo H et al (2009) Enterobacter oryzae sp. nov., a nitrogen-fixing bacterium isolated from the wild rice species Oryza latifolia. Int J Syst Evol Microbiol 59:1650–1655. https://doi.org/10.1099/ijs.0.65484-0
Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya 17:362–370
Piwpuan N, Zhai X, Brix H (2013) Nitrogen nutrition of Cyperus laevigatus and Phormium tenax: effects of ammonium versus nitrate on growth, nitrate reductase activity and N uptake kinetics. Aquat Bot 106:42–51. https://doi.org/10.1016/j.aquabot.2009.11.004
Poli A, Esposito E, Orlando P et al (2007) Halomonas alkaliantarctica sp. nov., isolated from saline lake Cape Russell in Antarctica, an alkalophilic moderately halophilic, exopolysaccharide-producing bacterium. Syst Appl Microbiol 30:31–38. https://doi.org/10.1016/j.syapm.2006.03.003
Premono ME, Moawad AM, Vlek PLG (1996) Effect of phosphate-solubilizing Pseudomonas putida on the growth of maize and its survival in the rhizosphere. Indones J Crop Sci 11(1):13–23
Provin T, Pit JL (2001) Managing soil salinity. In: AgriLIFE EXTENSION Texas A&M University System. https://oaktrust.library.tamu.edu/bitstream/handle/1969.1/86985/pdf_1397.pdf?sequence=1. p E60. Accessed 16 Dec 2021
Puri A, Padda KP, Chanway CP (2017) Beneficial effects of bacterial endophytes on forest tree species. In: Maheshwari DK, Annapurna K (eds) Endophytes: Crop productivity and protection, sustainable development and biodiversity, vol 16. Springer International Publishing, pp 111–132
Qadir M, Quillérou E, Nangia V et al (2014) Economics of salt-induced land degradation and restoration. Nat Resour Forum 38:282–295. https://doi.org/10.1111/1477-8947.12054
Radhakrishnan R, Lee IJ (2013) Regulation of salicylic acid, jasmonic acid and fatty acids in cucumber (Cucumis sativus L.) by spermidine promotes plant growth against salt stress. Acta Physiol Plant 35:3315–3322. https://doi.org/10.1007/s11738-013-1364-0
Radhakrishnan R, Hashem A, Abd Allah EF (2017) Bacillus: a biological tool for crop improvement through bio-molecular changes in adverse environments. Front Physiol 8:667. https://doi.org/10.3389/fphys.2017.00667
Rahman MH, Saiga S (2007) Endophyte effects on nutrient acquisition in tall fescue grown in andisols. J Plant Nutr 30:2141–2158. https://doi.org/10.1080/01904160701700632
Raichand R, Pareek S, Singh NK, Mayilraj S (2012) Exiguobacterium aquaticum sp. nov., a member of the genus Exiguobacterium. Int J Syst Evol Microbiol 62:2150–2155. https://doi.org/10.1099/ijs.0.035790-0
Ramadan T (2001) Dynamics of salt secretion by Sporobolus spicatus (Vahl) kunth from sites of differing salinity. Ann Bot 87:259–266. https://doi.org/10.1006/anbo.2001.1326
Ramette A, Moënne-Loccoz Y, Défago G (2003) Prevalence of fluorescent pseudomonads producing antifungal phloroglucinols and/or hydrogen cyanide in soils naturally suppressive or conducive to tobacco black root rot. FEMS Microbiol Ecol 44:35–43. https://doi.org/10.1016/S0168-6496(02)00454-3
Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339. https://doi.org/10.1007/s11104-009-9895-2
Rijavec T, Lapanje A (2017) Cyanogenic Pseudomonas spp. strains are concentrated in the rhizosphere of alpine pioneer plants. Microbiol Res 194:20–28. https://doi.org/10.1016/j.micres.2016.09.001
Robertson GP, Vitousek PM (2009) Nitrogen in agriculture: balancing the cost of an essential resource. Annu Rev Environ Resour 34:97–125. https://doi.org/10.1146/annurev.environ.032108.105046
Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339. https://doi.org/10.1016/S0734-9750(99)00014-2
Ryu RJ, Patten CL (2008) Aromatic amino acid-dependent expression of indole-3-pyruvate decarboxylase is regulated by TyrR in Enterobacter cloacae UW5. J Bacteriol 190:7200–7208. https://doi.org/10.1128/JB.00804-08
Schumann P, Cui X, Stackebrandt E et al (2004) Jonesia quinghaiensis sp. nov., a new member of the suborder Micrococcineae. Int J Syst Evol Microbiol 54:2181–2184. https://doi.org/10.1099/ijs.0.63223-0
Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus 2:1–14. https://doi.org/10.1186/2193-1801-2-587
Sharma S, Kulkarni J, Jha B (2016) Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front Microbiol 7:1600. https://doi.org/10.3389/fmicb.2016.01600
Shi D, Sheng Y (2005) Effect of various salt-alkaline mixed stress conditions on sunflower seedlings and analysis of their stress factors. Environ Exp Bot 54:8–21. https://doi.org/10.1016/j.envexpbot.2004.05.003
Simachew A, Lanzén A, Gessesse A, Øvreås L (2016) Prokaryotic community diversity along an increasing salt gradient in a soda ash concentration pond. Microb Ecol 71:326–338. https://doi.org/10.1007/s00248-015-0675-7
Singh NK, Raichand R, Kaur I et al (2013a) Exiguobacterium himgiriensis sp. nov. a novel member of the genus Exiguobacterium, isolated from the Indian Himalayas. Antonie Van Leeuwenhoek 103:789–796. https://doi.org/10.1007/s10482-012-9861-5
Singh VK, Kavita K, Prabhakaran R, Jha B (2013b) Cis-9-octadecenoic acid from the rhizospheric bacterium Stenotrophomonas maltophilia BJ01 shows quorum quenching and anti-biofilm activities. Biofouling 29:855–867. https://doi.org/10.1080/08927014.2013.807914
Singh S, Kumar V, Dhanjal DS et al (2019) Endophytic microbes in abiotic stress management. Microb Endophytes Prospect Sustain Agric. https://doi.org/10.1016/B978-0-12-818734-0.00005-X
Tan L, Qu Y, Zhou J et al (2009) Identification and characteristics of a novel salt-tolerant Exiguobacterium sp. for azo dyes decolorization. Appl Biochem Biotechnol 159:728–738. https://doi.org/10.1007/s12010-009-8546-7
Teale WD, Paponov IA, Palme K (2006) Auxin in action: Signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859. https://doi.org/10.1038/nrm2020
Tiwari S, Singh P, Tiwari R et al (2011) Salt-tolerant rhizobacteria-mediated induced tolerance in wheat (Triticum aestivum) and chemical diversity in rhizosphere enhance plant growth. Biol Fertil Soils 47:907–916. https://doi.org/10.1007/s00374-011-0598-5
Vaishnav A, Varma A, Tuteja N, Choudhary DK (2017) Characterization of bacterial volatiles and their impact on plant health under abiotic stress. In: Choudhary DK et al (eds) Volatiles and food security. Springer Nature, Singapore, pp 15–24
Vaneechoutte M, Rossau R, De Vos P et al (1992) Rapid identification of bacteria of the Comamonadaceae with amplified ribosomal DNA-restriction analysis (ARDRA). FEMS Microbiol Lett 93:227–233. https://doi.org/10.1111/j.1574-6968.1992.tb05102.x
Vardharajula S, Ali SZ, Grover M et al (2011) Drought-tolerant plant growth promoting bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 6:1–14. https://doi.org/10.1080/17429145.2010.535178
Vishnivetskaya TA, Lucas S, Copeland A et al (2011) Complete genome sequence of the thermophilic bacterium Exiguobacterium sp. AT1b. J Bacteriol 193:2880–2881
Wang S, Ouyang L, Ju X et al (2014) Survey of plant drought-resistance promoting bacteria from populus euphratica tree living in arid area. Indian J Microbiol 54:419–426. https://doi.org/10.1007/s12088-014-0479-3
White JF, Kingsley KL, Zhang Q et al (2019) Review: endophytic microbes and their potential applications in crop management. Pest Manag Sci 75:2558–2565. https://doi.org/10.1002/ps.5527
Wolf A, Fritze A, Hagemann M, Berg G (2002) Stenotrophomonas rhizophila sp. nov., a novel plant-associated bacterium with antifungal properties. Int J Syst Evol Microbiol 52:1937–1944
Yañez-Yazlle MF, Romano-Armada N, Rajal VB, Irazusta VP (2021) Amelioration of saline stress on Chia (Salvia hispanica L.) seedlings inoculated with halotolerant plant growth-promoting bacteria isolated from hypersaline environments. Front Agron 3:1–14. https://doi.org/10.3389/fagro.2021.665798
Yang XD, Ali A, Xu YL et al (2019) Soil moisture and salinity as main drivers of soil respiration across natural xeromorphic vegetation and agricultural lands in an arid desert region. CATENA 177:126–133. https://doi.org/10.1016/j.catena.2019.02.015
Yao LJ, Shen YY, Zhan JP et al (2012) Rhizobium taibaishanense sp. nov., isolated from a root nodule of Kummerowia striata. Int J Syst Evol Microbiol 62:335–341
Yi H, Srinivasan S, Kim MK (2010) Stenotrophomonas panacihumi sp. nov., isolated from soil of a ginseng field. J Microbiol 48:30–35. https://doi.org/10.1007/s12275-010-0006-0
Yumoto I, Yamazaki K, Hishinuma M et al (2001) Pseudomonas alcaliphila sp. nov., a novel facultatively psychrophilic alkaliphile isolated from seawater. Int J Syst Evol Microbiol 51:349–355
Zamin M, Khattak AM (2017) Performance of Sporobolus spicatus ecotypes, UAE native grass, under various salinity levels. Pure Appl Biol 6:595–604
Zamin M, Khattak AM, Alyafei MA et al (2018) Sporobolus spicatus, a potential turf grass under the climatic conditions of United Arab Emirates. J Sci Agric 2:1–8
Zheng BX, Zhang DP, Wang Y et al (2019) Responses to soil pH gradients of inorganic phosphate solubilizing bacteria community. Sci Rep 9:25. https://doi.org/10.1038/s41598-018-37003-w
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Enquahone, S., van Marle, G. & Simachew, A. Plant growth-promoting characteristics of halotolerant endophytic bacteria isolated from Sporobolus specatus (Vahr) Kunth and Cyperus laevigatus L. of Ethiopian rift valley lakes. Arch Microbiol 204, 403 (2022). https://doi.org/10.1007/s00203-022-03021-6
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DOI: https://doi.org/10.1007/s00203-022-03021-6