Please wait a minute...
Journal of Arid Land
Journal of Arid Land  2020, Vol. 12 Issue (5): 730-740    DOI: 10.1007/s40333-020-0019-4     CSTR: 32276.14.s40333-020-0019-4
Research article     
Endophytic bacteria associated with halophyte Seidlitzia rosmarinus Ehrenb. ex Boiss. from saline soil of Uzbekistan and their plant beneficial traits
Vyacheslav SHURIGIN1,*(), Dilfuza EGAMBERDIEVA2,3, LI Li2, Kakhramon DAVRANOV4, Hovik PANOSYAN5, Nils-Kåre BIRKELAND6, Stephan WIRTH3, Sonoko D BELLINGRATH-KIMURA3,7
1Faculty of Biology, National University of Uzbekistan, Tashkent 100174, Uzbekistan
2Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China
3Leibniz Centre for Agricultural Landscape Research (ZALF), Müncheberg 15374, Germany
4Institute of Microbiology of the Academy of Sciences of the Republic of Uzbekistan, Tashkent 100128, Uzbekistan
5Department of Biochemistry, Microbiology and Biotechnology, Yerevan State University, Yerevan 0025, Armenia
6Department of Biological Sciences, University of Bergen, NO-5020 Bergen 7803, Norway
7Faculty of Life Science, Humboldt University of Berlin, Berlin 14195, Germany
Download: HTML     PDF(423KB)
Export: BibTeX | EndNote (RIS)      

Abstract  

Endophytic bacteria of halophytic plants play essential roles in salt stress tolerance. Therefore, an understanding of the true nature of plant-microbe interactions under extreme conditions is essential. The current study aimed to identify cultivable endophytic bacteria associated with the roots and shoots of Seidlitzia rosmarinus Ehrenb. ex Boiss. grown in the salt-affected soil in Uzbekistan and to evaluate their plant beneficial traits related to plant growth stimulation and stress tolerance. Bacteria were isolated from the roots and the shoots of S. rosmarinus using culture-dependent techniques and identified by the 16S rRNA gene. RFLP (Restriction Fragment Length Polymorphism) analysis was conducted to eliminate similar isolates. Results showed that the isolates from the roots of S. rosmarinus belonged to the genera Rothia, Kocuria, Pseudomonas, Staphylococcus, Paenibacillus and Brevibacterium. The bacterial isolates from the shoots of S. rosmarinus belonged to the genera Staphylococcus, Rothia, Stenotrophomonas, Brevibacterium, Halomonas, Planococcus, Planomicrobium and Pseudomonas, which differed from those of the roots. Notably, Staphylococcus, Rothia and Brevibacterium were detected in both roots and shoots, indicating possible migration of some species from roots to shoots. The root-associated bacteria showed higher levels of IAA (indole-3-acetic acid) synthesis compared with those isolated from the shoots, as well as the higher production of ACC (1-aminocyclopropane-1-carboxylate) deaminase. Our findings suggest that halophytic plants are valuable sources for the selection of microbes with a potential to improve plant fitness under saline soils.

Key words： endophytic bacteria      phylogenetic analysis      halophyte      auxin      plant beneficial traits     
Received: 26 February 2020      Published: 10 September 2020
Corresponding Authors:
About author: *Corresponding author: Vyacheslav SHURIGIN (E-mail: slaventus87@inbox.ru)
Service
E-mail this article
Add to my bookshelf
Add to citation manager
E-mail Alert
RSS
Articles by authors
SHURIGIN Vyacheslav
EGAMBERDIEVA Dilfuza
Li LI
DAVRANOV Kakhramon
PANOSYAN Hovik
BIRKELAND Nils-Kåre
WIRTH Stephan
D BELLINGRATH-KIMURA Sonoko
Cite this article:

Vyacheslav SHURIGIN, Dilfuza EGAMBERDIEVA, LI Li, Kakhramon DAVRANOV, Hovik PANOSYAN, Nils-Kåre BIRKELAND, Stephan WIRTH, Sonoko D BELLINGRATH-KIMURA. Endophytic bacteria associated with halophyte Seidlitzia rosmarinus Ehrenb. ex Boiss. from saline soil of Uzbekistan and their plant beneficial traits. Journal of Arid Land, 2020, 12(5): 730-740.

URL:

http://jal.xjegi.com/10.1007/s40333-020-0019-4     OR     http://jal.xjegi.com/Y2020/V12/I5/730

Fig. 1 Seidlitzia rosmarinus growing on saline soil in the Surkhandarya Province, Uzbekistan
Isolated strain sequence Closest match among bacteria (16S rRNA gene)
Strain Length (bp) Accession
number		 Species Accession number Identity (%)
JRT1 1452 MH311985 Rothia terrae NR_043968 99.1
JRT2 1450 MH311986 Kocuria palustris NR_026451 98.9
JRT3 1452 MH311987 Pseudomonas baetica NR_116899 98.9
JRT4 1450 MH311988 Staphylococcus warneri NR_025922 99.1
JRT5 1471 MH311989 Staphylococcus epidermidis NR_113957 99.1
JRT6 1460 MH311990 Paenibacillus amylolyticus NR_025882 98.7
JRT7 1466 MH311991 Brevibacterium frigoritolerans NR_115064 99.6
Table 1 Sequence similarities of endophytic bacteria isolated from the roots of Seidlitzia rosmarinus with sequences registered in GenBank
Isolated strain sequence Closest match among bacteria (16S rRNA gene)
Strain Length (bp) Accession
number		 Species Accession number Identity (%)
JST1 1474 MH311992 Staphylococcus warneri NR_025922 99.6
JST2 1445 MH311993 Rothia terrae NR_043968 98.7
JST3 1467 MH311994 Stenotrophomonas pavanii NR_118008 98.4
JST4 1474 MH311995 Staphylococcus succinus NR_028667 98.6
JST5 1471 MH311996 Brevibacterium frigoritolerans NR_115064 99.4
JST6 1458 MH311997 Staphylococcus epidermidis NR_113957 99.4
JST7 1442 MH311998 Halomonas sulfidaeris NR_027185 98.8
JST8 1478 MH311999 Planococcus salinarum NR_116802 98.7
JST9 1471 MH312000 Planomicrobium koreense NR_025011 98.5
JST10 1476 MH312001 Planococcus halocryophilus NR_118149 98.9
JST11 1454 MH312002 Planomicrobium soli NR_134133 98.5
JST12 1464 MH312003 Pseudomonas fluorescens NR_115715 98.6
Table 2 Sequence similarities of endophytic bacteria isolated from the shoots of Seidlitzia rosmarinus with sequences registered in GenBank
Fig. 2 Neighbor-joining phylogenetic tree based on 16S rRNA gene sequences isolated from endophytic bacteria of Seidlitzia rosmarinus, showing the relationship of isolated strains to their closest relatives in GenBank. All presented strains were divided into three groups: Firmicutes, Actinobacteria and Proteobacteria.

Isolated strain		 IAA production
(μg/mL)		 ACC
deaminase		 Plant growth stimulation (cm) Seed germination percentage (%)
Tr- Tr+ Roots Shoots
R. terrae JRT1 8.4±0.7 11.7±1.0 + 5.2±0.5* 5.4±0.5 89±4
K. palustris JRT2 8.9±0.7 12.5±0.8 + 5.4±0.6* 5.5±0.6 90±6
P. baetica JRT3 10.1±0.8 14.9±1.0 + 5.5±0.5* 5.5±0.6 92±5
S. warneri JRT4 3.8±0.4 4.0±0.4 - 4.7±0.5 4.8±0.5 82±5
S. epidermidis JRT5 4.8±0.5 8.9±0.5 - 4.9±0.5 5.1±0.5 85±5
P. amylolyticus JRT6 11.4±0.9 15.8±1.1 + 5.4±0.6* 5.5±0.5 91±6
B. frigoritolerans JRT7 0.0 0.0 + 4.8±0.5 5.1±0.5 85±6
S. warneri JST1 0.0 0.8±0.4 - 4.6±0.4 5.0±0.5 85±5
R. terrae JST2 8.4±0.7 11.7±1.0 + 5.2±0.5* 5.4±0.5 89±5
S. pavanii JST3 9.5±0.7 20.5±0.9 + 5.5±0.6* 5.6±0.6* 93±4
S. succinus JST4 7.1±0.6 10.9±0.9 - 5.1±0.5 5.3±0.5 87±6
B. frigoritolerans JST5 0.0 0.0 + 4.9±0.5 5.2±0.4 85±5
S. epidermidis JST6 3.3±0.5 6.5±0.5 - 4.7±0.4 5.1±0.5 85±4
H. sulfidaeris JST7 0.0 1.7±0.8 + 4.9±0.5 5.1±0.4 85±4
P. salinarum JST8 0.0 0.0 - 4.6±0.5 4.9±0.4 83±5
P. koreense JST9 7.8±0.7 9.9±0.9 + 5.1±0.6 5.3±0.6 88±6
P. halocryophilus JST10 0.0 1.0±0.4 - 4.7±0.4 5.0±0.5 85±5
P. soli JST11 9.3±0.7 12.3±0.8 + 5.4±0.5* 5.4±0.5 90±6
P. fluorescens JST12 7.2±1.3 11.6±1.5 + 5.6±0.6* 5.7±0.6* 94±4
Control 4.8±0.5 5.1±0.5 85±5
Table 3 Production of IAA (indole-3-acetic acid) and ACC (1-aminocyclopropane-1-carboxylate) deaminase activities in endophytic isolates of Seidlitzia rosmarinus and plant growth promoting abilities
[1]   Announ N, Mattei J, Jaoua S, et al. 2004. Multifocal discitis caused by Staphylococcus warneri. Joint Bone Spine, 71(3): 240-242.
doi: 10.1016/S1297-319X(03)00126-X pmid: 15182799
[2]   Bano N, Musarrat J. 2003. Characterization of a new Pseudomonas aeruginosa strain NJ-15 as a potential biocontrol agent. Current Microbiology, 46(5): 324-328.
doi: 10.1007/s00284-002-3857-8 pmid: 12732958
[3]   Barigye R, Schaan L, Gibbs P S, et al. 2007. Diagnostic evidence of Staphylococcus warneri as a possible cause of bovine abortion. Journal of Veterinary Diagnostic Investigation, 19(6): 694-696.
pmid: 17998560
[4]   Bulgarelli D, Schlaeppi K, Spaepen S, et al. 2013. Structure and functions of the bacterial microbiota of plants. Annual Review of Plant Biology, 64: 807-838.
doi: 10.1146/annurev-arplant-050312-120106 pmid: 23373698
[5]   Chi F, Shen S H, Cheng H P, et al. 2005. Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Applied and Environmental Microbiology, 71(11): 7271-7278.
[6]   Cho S T, Chang H H, Egamberdieva D, et al. 2015. Genome analysis of Pseudomonas fluorescens PCL1751: a rhizobacterium that controls root diseases and alleviates salt stress for its plant host. PLoS ONE, 10(10): e0140231.
doi: 10.1371/journal.pone.0140231 pmid: 26452056
[7]   Chou Y J, Chou J H, Lin K Y, et al. 2008. Rothia terrae sp. nov. isolated from soil in Taiwan. International Journal of Systematic and Evolutionary Microbiology, 58(1): 84-88.
[8]   Dashti A A, Jadaon M M, Abdulsamad A M, et al. 2009. Heat treatment of bacteria: a simple method of DNA extraction for molecular techniques. Kuwait Medical Journal, 41(2): 117-122.
[9]   Egamberdieva D, Kamilova F, Validov S, et al. 2008. High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown in salinated soil in Uzbekistan. Environmental Microbiology, 10(1): 1-9.
doi: 10.1111/j.1462-2920.2007.01424.x pmid: 18211262
[10]   Egamberdieva D, Kucharova Z, Davranov K, et al. 2011. Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biology and Fertility of Soils, 47: 197-205.
[11]   Egamberdieva D, Li L, Lindström K, et al. 2015. A synergistic interaction between salt tolerant Pseudomonas and Mesorhizobium strains improves growth and symbiotic performance of liquorice (Glycyrrhiza uralensis Fish.) under salt stress. Applied Microbiology and Biotechnology, 100: 2829-2841.
doi: 10.1007/s00253-015-7147-3 pmid: 26585446
[12]   Egamberdieva D, Li L, Wirth S, et al. 2017. Microbial cooperation in the rhizosphere improves liquorice growth under salt stress. Bioengineered, 8(4): 433-438.
pmid: 27780398
[13]   Egamberdieva D, Wirth S J, Behrendt U, et al. 2017a. Antimicrobial activity of medicinal plants correlates with the proportion of antagonistic endophytes. Frontiers in Microbiology, 8: 199.
doi: 10.3389/fmicb.2017.00199 pmid: 28232827
[14]   Egamberdieva D, Wirth S J, Shurigin V V, et al. 2017b. Endophytic bacteria improve plant growth, symbiotic performance of chickpea (Cicer arietinum L.) and induce suppression of root rot caused by Fusarium solani under salt stress. Frontiers in Microbiology, 8: 1887.
doi: 10.3389/fmicb.2017.01887 pmid: 29033922
[15]   Egamberdieva D, Wirth S J, Alqarawi A A, et al. 2017c. Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Frontiers in Microbiology, 8: 2104.
doi: 10.3389/fmicb.2017.02104 pmid: 29163398
[16]   El Shaer H M. 2010. Halophytes and salt-tolerant plants as potential forage for ruminants in the Near East region. Small Ruminant Research, 91(1): 3-12.
doi: 10.1016/j.smallrumres.2010.01.010
[17]   Etesami H, Beattie G A. 2017. Plant-microbe interactions in adaptation of agricultural crops to abiotic stress conditions. In: Kumar V, Kumar M, Sharma S, et al. Probiotics and Plant Health. Singapore: Springer, 163-200.
[18]   Etesami H, Beattie G A. 2018. Mining halophytes for plant growth-promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Frontiers in Microbiology, 9: 148.
doi: 10.3389/fmicb.2018.00148 pmid: 29472908
[19]   Felsenstein J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39(4): 783-791.
doi: 10.1111/j.1558-5646.1985.tb00420.x
[20]   Flowers T J, Colmer T D. 2015. Plant salt tolerance: Adaptations in halophytes. Annals of Botany, 115(3): 327-331.
doi: 10.1093/aob/mcu267 pmid: 25844430
[21]   Glick B R. 2014. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiological Research, 169(1): 30-39.
doi: 10.1016/j.micres.2013.09.009 pmid: 24095256
[22]   Grigore M N, Ivanescu L, Toma C. 2014. Halophytes: An Integrative Anatomical Study. New York: Springer, 39-43.
[23]   Gupta S, Pandey S. 2019. ACC deaminase producing bacteria with multifarious plant growth promoting traits alleviates salinity stress in French bean (Phaseolus vulgaris) plants. Frontiers in Microbiology, 10: 1506.
doi: 10.3389/fmicb.2019.01506 pmid: 31338077
[24]   Hadi M R. 2009. Biotechnological potentials of Seidlitzia rosmarinus: A mini review. African Journal of Biotechnology, 8(11): 2429-2431.
[25]   Hasanuzzaman M, Nahar K, Alam M, et al. 2014. Potential use of halophytes to remediate saline soils. BioMed Research International, 589341.
doi: 10.1155/2014/589341 pmid: 25110683
[26]   Hashem A, Abd Allah E F, Alqarawi A, et al. 2016. The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Frontiers in Microbiology, 7: 1089.
doi: 10.3389/fmicb.2016.01089 pmid: 27486442
[27]   Jha B, Gontia I, Hartmann A. 2012. The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant and Soil, 356: 265-277.
[28]   Jinneman K C, Wetherington J H, Adams A M, et al. 1996. Differentiation of Cyclospora sp. and Eimeria spp. by using the polymerase chain reaction amplification products and restriction fragment length polymorphisms. Food and Drug Administration Laboratory Information Bulletin, 4044.
[29]   Kaplan D, Maymon M, Agapakis C M, et al. 2013. A survey of the microbial community in the rhizosphere of two dominant shrubs of the Negev Desert highlands, Zygophyllum dumosum (Zygophyllaceae) and Atriplex halimus (Amaranthaceae), using cultivation-dependent and cultivation-independent methods. American Journal of Botany, 100: 1713-1725.
doi: 10.3732/ajb.1200615 pmid: 23975635
[30]   Kaye J Z, Baross J A. 2000. High incidence of halotolerant bacteria in Pacific hydrothermal-vent and pelagic environments. FEMS Microbiology Ecology, 32(3): 249-260.
doi: 10.1111/j.1574-6941.2000.tb00718.x pmid: 10858584
[31]   Kloos W E, Schleifer K H. 1975. Isolation and characterization of staphylococci from human skin II. descriptions of four new species: Staphylococcus warneri, Staphylococcus capitis, Staphylococcus hominis, and Staphylococcus simulans. International Journal of Systematic Bacteriology, 25(1): 62-79.
[32]   Kurkova E B, Kalinkina L G, Baburina O K, et al. 2002. Responses of Seidlitzia rosmarinus to salt stress. Biology Bulletin of the Russian Academy of Sciences, 29: 221-229.
[33]   Lane D J. 1991. 16S/23S rRNA Sequencing. In: Stackebrandt E, Goodfellow M. Nucleic Acid Techniques in Bacterial Systematic, New York: John Wiley and Sons, 115-175.
[34]   Ludwig-Mueller J. 2015. Plants and endophytes: equal partners in secondary metabolite production? Biotechnology Letters, 37: 1325-1334.
doi: 10.1007/s10529-015-1814-4 pmid: 25792513
[35]   Luo X, Zhang J, Li D, et al. 2014. Planomicrobium soli sp. nov., isolated from soil. International Journal of Systematic and Evolutionary Microbiology, 64: 2700-2705.
pmid: 24854007
[36]   Mishra A, Tanna B. 2017. Halophytes: potential resources for salt stress tolerance genes and promoters. Frontiers in Plant Science, 8: 829.
doi: 10.3389/fpls.2017.00829 pmid: 28572812
[37]   Mora-Ruiz M D R, Font-Verdera F, Díaz-Gil C, et al. 2015. Moderate halophilic bacteria colonizing the phylloplane of halophytes of the subfamily Salicornioideae (Amaranthaceae). Systematic and Applied Microbiology, 38(6): 406-416.
doi: 10.1016/j.syapm.2015.05.004 pmid: 26164126
[38]   Mora-Ruiz M D R, Font-Verdera F, Orfila A, et al. 2016. Endophytic microbial diversity of the halophyte Arthrocnemum macrostachyum across plant compartments. FEMS Microbiology Ecology, 92(9): fiw145.
doi: 10.1093/femsec/fiw115 pmid: 27242370
[39]   Muchate N S, Nikalje G C, Rajurkar N S, et al. 2016. Plant salt stress: adaptive responses, tolerance mechanism and bioengineering for salt tolerance. The Botanical Review, 82: 371-406.
[40]   Mykytczuk N C, Wilhelm R C, Whyte L G, 2012. Planococcus halocryophilus sp. nov., an extreme sub-zero species from high Arctic permafrost. International Journal of Systematic and Evolutionary Microbiology, 62: 1937-1944.
[41]   Nanjani S G, Soni H P. 2014. Characterization of an extremely halotolerant Staphylococcus arlettae HPSSN35C isolated from Dwarka Beach, India. Journal of Basic Microbiology, 53(8): 1-8.
[42]   Nováková D, Sedlácek I, Pantůcek R, et al. 2006. Staphylococcus equorum and Staphylococcus succinus isolated from human clinical specimens. Journal of Medical Microbiology, 55(5): 523-528.
[43]   Piccoli P, Travaglia C, Cohen A, et al. 2011. An endophytic bacterium isolated from roots of the halophyte Prosopis strombulifera produces ABA, IAA, gibberellins A1 and A3 and jasmonic acid in chemically-defined culture medium. Plant Growth Regulation, 64: 207-210.
[44]   Ramos P L, van Trappen S, Thompson F L, et al. 2011. Screening for endophytic nitrogen-fixing bacteria in Brazilian sugar cane varieties used in organic farming and description of Stenotrophomonas pavanii sp. nov. International Journal of Systematic and Evolutionary Microbiology, 61(4): 926-931.
[45]   Rashid S, Charles T C, Glick B R. 2012. Isolation and characterization of new plant growth-promoting bacterial endophytes. Applied Soil Ecology, 61(4): 217-224.
[46]   Roohi A, Ahmed I, Iqbal M, et al. 2012. Preliminary isolation and characterization of halotolerant and halophilic bacteria from salt mines of Karak. Pakistan Journal of Botany, 44: 365-370.
[47]   Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4): 406-425.
doi: 10.1093/oxfordjournals.molbev.a040454 pmid: 3447015
[48]   Sgroy V, Cassan F, Masciarelli O, et al. 2009. Isolation and characterization of endophytic plant growth‐promoting (PGPB) or stress homeostasis‐regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Applied Microbiology and Biotechnology, 85(2): 371-381.
doi: 10.1007/s00253-009-2116-3 pmid: 19655138
[49]   Sorty A M, Meena K K, Choudhary K, et al. 2016. Effect of plant growth promoting bacteria associated with halophytic weed (Psoralea corylifolia L.) on germination and seedling growth of wheat under saline conditions. Applied Biochemistry and Biotechnology, 180: 872-882.
doi: 10.1007/s12010-016-2139-z pmid: 27215915
[50]   Surette M A, Sturz A V, Lada R R, et al. 2003. Bacterial endophytes in processing carrots (Daucus carota L. var. sativus): their localization, population density, biodiversity and their effects on plant growth. Plant and Soil, 253: 381-390.
[51]   Szymańska S, Płociniczak T, Piotrowska-Seget Z, et al. 2016. Metabolic potential and community structure of endophytic and rhizosphere bacteria associated with the roots of the halophyte Aster tripolium L. Microbiological Research, 182: 68-79.
doi: 10.1016/j.micres.2015.09.007 pmid: 26686615
[52]   Tamura K, Nei M, Kumar S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences of the United States of America, 101(30): 11030-11035.
[53]   Tamura K, Stecher G, Peterson D, et al. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12): 2725-2729.
doi: 10.1093/molbev/mst197 pmid: 24132122
[54]   Toderich K N, Ismail S, Juylova E A, et al. 2008. New approaches for Biosaline Agriculture development, management and conservation of sandy desert ecosystems. In: Chedly A, Munir O, Muhamad A, et al. Biosaline Agriculture and Salinity Tolerance in Plant. Basel: Birkhauser Verlag, 247-264.
[55]   Valverde A, Igual J M, Santa R I, et al. 2005. Preliminary diversity studies of culturable phyllosphere bacteria on chestnut (Castanea sativa). Acta Horticulturae, 693: 263-270.
[56]   Yoon J H, Kang S S, Lee K C, et al. 2001. Planomicrobium koreense gen. nov., sp. nov., a bacterium isolated from the Korean traditional fermented seafood jeotgal, and transfer of Planococcus okeanokoites (Nakagawa et al., 1996) and Planococcus mcmeekinii (Junge et al., 1998) to the genus Planomicrobium. International Journal of Systematic and Evolutionary Microbiology, 51: 1511-1520.
doi: 10.1099/00207713-51-4-1511 pmid: 11491353
[57]   Yoon J H, Kang S J, Lee S Y, et al. 2010. Planococcus salinarum sp. nov., isolated from a marine solar saltern, and emended description of the genus Planococcus. International Journal of Systematic and Evolutionary Microbiology, 60(4): 754-758.
[58]   You Y H, Park M J, Lee M C, et al. 2015. Characterization and phylogenetic analysis of halophilic bacteria isolated from rhizosphere soils of coastal plants in Dokdo Islands. Korean Journal of Microbiology, 51(1): 86-95.
[59]   Zhao S, Zhou N, Zhao Z Y, et al. 2016. Isolation of endophytic plant growth-promoting bacteria associated with the halophyte Salicornia europaea and evaluation of their promoting activity under salt stress. Current Microbiology, 73(4): 574-581.
doi: 10.1007/s00284-016-1096-7 pmid: 27447799
[1] DU Lan, TIAN Shengchuan, ZHAO Nan, ZHANG Bin, MU Xiaohan, TANG Lisong, ZHENG Xinjun, LI Yan. Climate and topography regulate the spatial pattern of soil salinization and its effects on shrub community structure in Northwest China[J]. Journal of Arid Land, 2024, 16(7): 925-942.
[2] YANG Ao, TU Wenqin, YIN Benfeng, ZHANG Shujun, ZHANG Xinyu, ZHANG Qing, HUANG Yunjie, HAN Zhili, YANG Ziyue, ZHOU Xiaobing, ZHUANG Weiwei, ZHANG Yuanming. Predicting changes in the suitable habitats of six halophytic plant species in the arid areas of Northwest China[J]. Journal of Arid Land, 2024, 16(10): 1380-1408.
[3] ZHAO Mengqi, SU Huan, HUANG Yin, Rashidin ABDUGHENI, MA Jinbiao, GAO Jiangtao, GUO Fei, LI Li. Plant growth-promoting properties and anti-fungal activity of endophytic bacterial strains isolated from Thymus altaicus and Salvia deserta in arid lands[J]. Journal of Arid Land, 2023, 15(11): 1405-1420.
[4] LI Li, GAO Lei, LIU Yonghong, FANG Baozhu, HUANG Yin, Osama A A MOHAMAD, Dilfuza EGAMBERDIEVA, LI Wenjun, MA Jinbiao. Diversity of cultivable endophytic bacteria associated with halophytes in Xinjiang of China and their plant beneficial traits[J]. Journal of Arid Land, 2021, 13(8): 790-800.
[5] Syed Z SHAH, Aysha RASHEED, Bilquees GUL, Muhammad A KHAN, Brent L NIELSEN, Abdul HAMEED. Maternal salinity improves yield, size and stress tolerance of Suaeda fruticosa seeds[J]. Journal of Arid Land, 2020, 12(2): 283-293.
[6] Yonghong LIU, Jianwei GUO, Li LI, D ASEM Mipeshwaree, Yongguang ZHANG, A MOHAMAD Osama, SALAM Nimaichand, Wenjun LI. Endophytic bacteria associated with endangered plant Ferula sinkiangensis K. M. Shen in an arid land: diversity and plant growth-promoting traits[J]. Journal of Arid Land, 2017, 9(3): 432-445.
[7] Ali EL-KEBLAWY, Sanjay GAIROLA, Arvind BHATT. Maternal salinity environment affects salt tolerance during germination in Anabasis setifera: A facultative desert halophyte[J]. Journal of Arid Land, 2016, 8(2): 254-263.
[8] Fei WANG, Xi CHEN, GePing LUO, JianLi DING, XianFeng CHEN. Detecting soil salinity with arid fraction integrated index and salinity index in feature space using Landsat TM imagery[J]. Journal of Arid Land, 2013, 5(3): 340-353.
[9] Ke ZHANG, ChunJian LI, ZhongShao LI, FuHai ZHANG, ZhenYong ZHAO, ChangYan TIAN. Characteristics of mineral elements in shoots of three annual halophytes in a saline desert, Northern Xinjiang[J]. Journal of Arid Land, 2013, 5(2): 244-254.
[10] JunFeng YUAN, ChangYan TIAN, Gu FENG. Effects of sodium on nitrate uptake and osmotic adjustment of Suaeda physophora[J]. Journal of Arid Land, 2010, 2(3): 190-196.