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Genomic features of a plant growth-promoting endophytic Enterobacter cancerogenus JY65 dominant in microbiota of halophyte Suaeda salsa

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Abstract

Amis

Plant growth-promoting bacteria (PGPB) are beneficial organisms that promote plant growth and increase plant tolerance to abiotic stresses. Many halophytes attract and recruit salt-tolerant microorganisms to enhance salt tolerance. However, little is known about the composition and ecological function of bacterial microbiota of Suaeda salsa.

Methods

Here, using a culture-dependent technique, we characterized the bacterial communities in the roots, stems, leaves, the rhizosphere, and bulk soils of S. salsa.

Results

We identified 71 representative bacterial strains belonging to 13 genera, with Enterobacter as the most dominant genus. All isolates produce indole-3-acetic acid (IAA) although the yields vary, have similar tolerance to alkaline pH up to 12 but varied salt tolerance. One strain JY65 isolated from the leaves showed the highest tolerance to salt stress. Addition of JY65 promoted growth of rice under NaCl stress with significantly increased plant biomass, plant height and root length. Up-regulated Na+ homeostasis-related gene expression and accumulation of antioxidant compounds was found in rice inoculated with JY65 strain. The strain was named as Enterobacter cancerogenus JY65 based on phylogenetic analysis. Genomic analysis of JY65 revealed existence of many PGP related genes such as IAA production, siderophore, nutrient uptake, and antimicrobial compounds. In addition, genes involved in adaptation to the harsh environment, including antioxidant enzyme, exopolysaccharide, osmoprotectant accumulation, ion homeostasis, were identified in JY65 genome.

Conclusions

These results provide novel insights into the composition of microbiota associated with halophyte S. salsa and revealed the mechanisms underlying the plant growth promotion of E. cancerogenus JY65.

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Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Ahmad P, Tripathi DK, Deshmukh R, Pratap Singh V, Corpas FJ (2019) Revisiting the role of ROS and RNS in plants under changing environment. Environ Exp Bot 161:1–3

    Article  CAS  Google Scholar 

  • Ajmal AW, Yasmin H, Hassan MN, Khan N, Jan BL, Mumtaz S (2022) Heavy metal-resistant plant growth-promoting Citrobacter werkmanii Strain WWN1 and enterobacter cloacae strain JWM6 enhance wheat (Triticum aestivum L.) growth by modulating physiological attributes and some key antioxidants under multi-metal stress. Front Microbiol 13:815704–815704

    Article  PubMed  PubMed Central  Google Scholar 

  • Al Hinai MS, Ullah A, Al-Rajhi RS, Farooq M (2022) Proline accumulation, ion homeostasis and antioxidant defence system alleviate salt stress and protect carbon assimilation in bread wheat genotypes of Omani origin. Environ Exp Bot 193:104687

    Article  Google Scholar 

  • Alishahi F, Alikhani HA, Khoshkholgh-Sima NA, Etesami H (2020) Mining the roots of various species of the halophyte Suaeda for halotolerant nitrogen-fixing endophytic bacteria with the potential for promoting plant growth. Int Microbiol 23:415–427

    Article  PubMed  CAS  Google Scholar 

  • Andrés-Barrao C, Lafi FF, Alam I, De Zélicourt A, Eida AA, Bokhari A, Alzubaidy H, Bajic VB, Hirt H, Saad MM (2017) Complete genome sequence analysis of Enterobacter sp. SA187, a plant multi-stress tolerance promoting endophytic bacterium. Front Microbiol 8:2023

    Article  PubMed  PubMed Central  Google Scholar 

  • Andrés-Barrao C, Alzubaidy H, Jalal R, Mariappan KG, de Zélicourt A, Bokhari A, Artyukh O, Alwutayd K, Rawat A, Shekhawat K (2021) Coordinated bacterial and plant sulfur metabolism in Enterobacter sp. SA187–induced plant salt stress tolerance. Proc Natl Acad Sci 118:e2107417118

    Article  PubMed  PubMed Central  Google Scholar 

  • Arora NK, Egamberdieva D, Mehnaz S, Li W-J, Mishra I (2021) Salt tolerant rhizobacteria: for better productivity and remediation of saline soils. Front Microbiol 12:848

    Article  Google Scholar 

  • Bavaresco LG, Osco LP, Araujo ASF, Mendes LW, Bonifacio A, Araújo FF (2020) Bacillus subtilis can modulate the growth and root architecture in soybean through volatile organic compounds. Theor Exp Plant Physiol 32:99–108

    Article  CAS  Google Scholar 

  • Bhise KK, Dandge PB (2019) Mitigation of salinity stress in plants using plant growth promoting bacteria. Symbiosis 79:191–204

    Article  Google Scholar 

  • Chin C-S, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10:563–569

    Article  PubMed  CAS  Google Scholar 

  • Christakis CA, Daskalogiannis G, Chatzaki A, Markakis EA, Mermigka G, Sagia A, Rizzo GF, Catara V, Lagkouvardos I, Studholme DJ (2021) Endophytic bacterial isolates from halophytes demonstrate phytopathogen biocontrol and plant growth promotion under high salinity. Front Microbiol 12:681567

    Article  PubMed  PubMed Central  Google Scholar 

  • Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678

    Article  CAS  Google Scholar 

  • Darling AC, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5:e11147

    Article  PubMed  PubMed Central  Google Scholar 

  • Daulay FR, Simarmata T (2021) Current status and prospect of halotolerant biofilm PGPR (plant growth promoting rhizobacteria) as bioagent to increase crops growth on saline soils. IOP Publ 748:012042

  • Duca DR, Glick BR (2020) Indole-3-acetic acid biosynthesis and its regulation in plant-associated bacteria. Appl Microbiol Biotechnol 104:8607–8619

    Article  PubMed  CAS  Google Scholar 

  • El-Tarabily KA, Ramadan GA, Elbadawi AA, Hassan AH, Tariq S, Ghazal EW, Abo Gamar MI, AbuQamar SF (2021) The marine endophytic polyamine-producing Streptomyces mutabilis UAE1 isolated from extreme niches in the Arabian Gulf promotes the performance of mangrove (Avicennia marina) seedlings under greenhouse conditions. Front Mar Sci 8:710200

    Article  Google Scholar 

  • Etesami H, Glick BR (2020) Halotolerant plant growth–promoting bacteria: prospects for alleviating salinity stress in plants. Environ Exp Bot 178:104124

    Article  CAS  Google Scholar 

  • Guo D-J, Singh RK, Singh P, Li D-P, Sharma A, Xing Y-X, Song X-P, Yang L-T, Li Y-R (2020) Complete genome sequence of Enterobacter roggenkampii ED5, a nitrogen fixing plant growth promoting endophytic bacterium with biocontrol and stress tolerance properties, isolated from sugarcane root. Front Microbiol 11:580081

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo J, Chen Y, Lu P, Liu M, Sun P, Zhang Z (2021) Roles of endophytic bacteria in Suaeda salsa grown in coastal wetlands: Plant growth characteristics and salt tolerance mechanisms. Environ Pollut 287:117641

    Article  PubMed  CAS  Google Scholar 

  • Haroon U, Liaquat F, Khizar M, Akbar M, Saleem H, Arif S, Ali W, Chaudhary HJ, Munis MFH (2021) Isolation of halotolerant bacteria from rhizosphere of Khewra salt mine halophytes and their application to induce salt tolerance in wheat. Geomicrobiol J 38:768–775

    Article  CAS  Google Scholar 

  • Ha-Tran DM, Nguyen TTM, Hung S-H, Huang E, Huang C-C (2021) Roles of plant growth-promoting rhizobacteria (PGPR) in stimulating salinity stress defense in plants: A review. Int J Mol Sci 22:3154

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hoque M, Hannan A, Imran S, Paul NC, Mondal M, Sadhin M, Rahman M, Bristi JM, Dola FS, Hanif M (2022) Plant growth-promoting rhizobacteria-mediated adaptive responses of plants under salinity stress. J Plant Growth Regul 42:1307–1326

    Article  Google Scholar 

  • Ibrahim EA (2016) Seed priming to alleviate salinity stress in germinating seeds. J Plant Physiol 192:38–46

    Article  PubMed  CAS  Google Scholar 

  • Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S (2018) High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 9:1–8

    Article  Google Scholar 

  • Jha CK, Patel B, Saraf M (2012) Stimulation of the growth of Jatropha curcas by the plant growth promoting bacterium Enterobacter cancerogenus MSA2. World J Microbiol Biotechnol 28:891–899

    Article  PubMed  CAS  Google Scholar 

  • Jia H, Xi Z, Ma J, Li Y, Hao C, Lu M, Zhang Z-Z, Deng W-W (2022) Endophytic bacteria from the leaves of two types of albino tea plants, indicating the plant growth promoting properties. Plant Growth Regul 96:331–343

    Article  CAS  Google Scholar 

  • Kearl J, McNary C, Lowman JS, Mei C, Aanderud ZT, Smith ST, West J, Colton E, Hamson M, Nielsen BL (2019) Salt-tolerant halophyte rhizosphere bacteria stimulate growth of alfalfa in salty soil. Front Microbiol 10:1849

    Article  PubMed  PubMed Central  Google Scholar 

  • Khabbaz SE, Ladhalakshmi D, Babu M, Kandan A, Ramamoorthy V, Saravanakumar D, Al-Mughrabi T, Kandasamy S (2019) Plant growth promoting bacteria (PGPB)—a versatile tool for plant health management. Can J Pestic Pest Manage 1:1–25

    Article  Google Scholar 

  • Khanna K, Kohli SK, Sharma A, Ohri P, Bhardwaj R, Al-Huqail AA, Siddiqui MH, Ahmad P (2020) Histochemical and physicochemical studies reveal improved defense in tomato under Cd stress with rhizobacterial supplementation. Plant Soil 446:393–411

    Article  CAS  Google Scholar 

  • Khanna K, Ohri P, Bhardwaj R, Ahmad P (2022) Unsnarling plausible role of plant growth-promoting rhizobacteria for mitigating Cd-Toxicity from plants: an environmental safety aspect. J Plant Growth Regul 41:2514–2542

    Article  CAS  Google Scholar 

  • Khanna K, Jamwal VL, Kohli SK, Gandhi SG, Ohri P, Bhardwaj R, Abd_Allah EF, Hashem A, Ahmad P (2019) Plant growth promoting rhizobacteria induced Cd tolerance in Lycopersicon esculentum through altered antioxidative defense expression. Chemosphere 217:463–474

  • Khanna K, Ohri P, Bhardwaj R, Ahmad P (2021) Unsnarling plausible role of plant growth-promoting rhizobacteria for mitigating Cd-toxicity from plants: an environmental safety aspect. J Plant Growth Regul 41:2514–2542

    Article  Google Scholar 

  • Khatoon Z, Huang S, Farooq MA, Santoyo G, Rafique M, Javed S, Gul B (2022) Role of plant growth-promoting bacteria (PGPB) in abiotic stress management. In: Mitigation of Plant Abiotic Stress by Microorganisms. Academic Press, pp 257–272. https://doi.org/10.1016/B978-0-323-90568-8.00012-2

  • Kohli SK, Khanna K, Bhardwaj R, Abd Allah EF, Ahmad P, Corpas FJ (2019) Assessment of subcellular ROS and NO metabolism in higher plants: multifunctional signaling molecules. Antioxidants (Basel) 8(12):641

    Article  PubMed  CAS  Google Scholar 

  • Krishnamoorthy A, Gupta A, Sar P, Maiti MK (2021) Metagenomics of two gnotobiotically grown aromatic rice cultivars reveals genotype-dependent and tissue-specific colonization of endophytic bacterial communities attributing multiple plant growth promoting traits. World J Microbiol Biotechnol 37:1–16

    Article  Google Scholar 

  • Kumawat KC, Sharma B, Nagpal S, Kumar A, Tiwari S, Nair RM (2023) Plant growth-promoting rhizobacteria: Salt stress alleviators to improve crop productivity for sustainable agriculture development. Front Plant Sci 13:1101862

    Article  PubMed  PubMed Central  Google Scholar 

  • Lahlali R, Ezrari S, Radouane N, Belabess Z, Jiang Y, Mokrini F, Tahiri A, Peng G (2022) Bacillus spp.-Mediated drought stress tolerance in plants: current and future prospects. In: Bacilli in Agrobiotechnology. Springer, Cham, pp 487–518

  • Laverty G, Gorman SP, Gilmore BF (2014) Biomolecular mechanisms of Pseudomonas aeruginosa and Escherichia coli biofilm formation. Pathogens 3:596–632

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Letunic I, Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49:W293–W296

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li H, Lei P, Pang X, Li S, Xu H, Xu Z, Feng X (2017) Enhanced tolerance to salt stress in canola (Brassica napus L.) seedlings inoculated with the halotolerant Enterobacter cloacae HSNJ4. Appl Soil Ecol 119:26–34

    Article  CAS  Google Scholar 

  • Li J, Chen Q, Li Q, Zhao C, Feng Y (2021) Influence of plants and environmental variables on the diversity of soil microbial communities in the Yellow River Delta Wetland, China. Chemosphere 274:129967

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Zhao H, Wu L, Liu A, Zhao FJ, Xu W (2017) Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytol 215:687–698

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Long HH, Sonntag DG, Schmidt DD, Baldwin IT (2010) The structure of the culturable root bacterial endophyte community of Nicotiana attenuata is organized by soil composition and host plant ethylene production and perception. New Phytol 185:554–567

    Article  PubMed  CAS  Google Scholar 

  • Lu L, Chang M, Han X, Wang Q, Wang J, Yang H, Guan Q, Dai S (2021) Beneficial effects of endophytic Pantoea ananatis with ability to promote rice growth under saline stress. J Appl Microbiol 131:1919–1931

    Article  PubMed  CAS  Google Scholar 

  • Ludueña LM, Anzuay MS, Angelini JG, McIntosh M, Becker A, Rupp O, Goesmann A, Blom J, Fabra A, Taurian T (2018) Genome sequence of the endophytic strain Enterobacter sp. J49, a potential biofertilizer for peanut and maize. Genomics 111:913–920

    Article  PubMed  Google Scholar 

  • Mansoor S, Ali Wani O, Lone JK, Manhas S, Kour N, Alam P, Ahmad A, Ahmad P (2022) Reactive oxygen species in plants: from source to sink. Antioxidants (Basel) 11(2):225

    Article  PubMed  CAS  Google Scholar 

  • Miliute I, Buzaite O, Baniulis D, Stanys V (2015) Bacterial endophytes in agricultural crops and their role in stress tolerance: a review. Zemdirbyste Agric 102:465–478

    Article  Google Scholar 

  • Mishra P, Mishra J, Arora NK (2021) Plant growth promoting bacteria for combating salinity stress in plants–recent developments and prospects: a review. Microbiol Res 252:126861

    Article  PubMed  CAS  Google Scholar 

  • Mukhtar S, Mehnaz S, Mirza MS, Malik KA (2019) Isolation and characterization of bacteria associated with the rhizosphere of halophytes (Salsola stocksii and Atriplex amnicola) for production of hydrolytic enzymes. Braz J Microbiol 50:85–97

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33:1–16

    Article  CAS  Google Scholar 

  • Pande A, Kaushik S, Pandey P, Negi A (2019) Isolation, characterization, and identification of phosphate-solubilizing Burkholderia cepacia from the sweet corn cv. Golden Bantam rhizosphere soil and effect on growth-promoting activities. Int J Veg Sci 26:591–607

    Article  Google Scholar 

  • Peng M, Wang C, Wang Z, Huang X, Zhou F, Yan S, Liu X (2022) Differences between the effects of plant species and compartments on microbiome composition in two halophyte Suaeda species. Bioengineered 13:12475–12488

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM (2016) Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza 26:673–684

    Article  PubMed  CAS  Google Scholar 

  • Qi G, Pan Z, Sugawa Y, Andriamanohiarisoamanana FJ, Yamashiro T, Iwasaki M, Kawamoto K, Ihara I, Umetsu K (2018) Comparative fertilizer properties of digestates from mesophilic and thermophilic anaerobic digestion of dairy manure: focusing on plant growth promoting bacteria (PGPB) and environmental risk. J Mater Cycles Waste Manage 20:1448–1457

    Article  CAS  Google Scholar 

  • Qin S, Miao Q, Feng W-W, Wang Y, Zhu X, Xing K, Jiang J-H (2015) Biodiversity and plant growth promoting traits of culturable endophytic actinobacteria associated with Jatropha curcas L. growing in Panxi dry-hot valley soil. Appl Soil Ecol 93:47–55

    Article  Google Scholar 

  • Qin S, Feng W-W, Zhang Y-J, Wang T-T, Xiong Y-W, Xing K (2018) Diversity of bacterial microbiota of coastal halophyte Limonium sinense and amelioration of salinity stress damage by symbiotic plant growth-promoting actinobacterium Glutamicibacter halophytocola KLBMP 5180. Appl Environ Microbiol 84:e01533-e1618

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rahman MM, Mostofa MG, Keya SS, Siddiqui MN, Ansary MMU, Das AK, Rahman MA, Tran LS-P (2021) Adaptive mechanisms of halophytes and their potential in improving salinity tolerance in plants. Int J Mol Sci 22:10733

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ranawat B, Mishra S, Singh A (2021) Enterobacter hormaechei (MF957335) enhanced yield, disease and salinity tolerance in tomato. Arch Microbiol 203:2659–2667

    Article  PubMed  CAS  Google Scholar 

  • Sagar A, Sayyed RZ, Ramteke PW, Sharma S, Marraiki N, Elgorban AM, Syed A (2020) ACC deaminase and antioxidant enzymes producing halophilic Enterobacter sp. PR14 promotes the growth of rice and millets under salinity stress. Physiol Mol Biol Plants 26:1847–1854

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Santoyo G, Moreno-Hagelsieb G, del Carmen O-M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99

    Article  PubMed  CAS  Google Scholar 

  • Saroy K, Garg N (2021) Role of non-enzymatic antioxidant defense mechanisms in imparting heavy metal, salt, water and temperature stress tolerance in plants. In: Organic solutes, oxidative stress, and antioxidant enzymes under abiotic stressors. CRC Press, Boca Raton, FL, pp 321–338

  • Shi W, Takano T, Liu S (2012) Isolation and characterization of novel bacterial taxa from extreme alkali-saline soil. World J Microbiol Biotechnol 28:2147–2157

    Article  PubMed  Google Scholar 

  • Song J, Wang B (2015) Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot 115:541–553

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tavanti TR, de Melo AAR, Moreira LDK, Sanchez DEJ, dos Santos SR, da Silva RM, Dos Reis AR (2021) Micronutrient fertilization enhances ROS scavenging system for alleviation of abiotic stresses in plants. Plant Physiol Biochem 160:386–396

    Article  PubMed  CAS  Google Scholar 

  • Thorne SJ, Hartley SE, Maathuis FJ (2020) Is silicon a panacea for alleviating drought and salt stress in crops? Front Plant Sci 11:1221

    Article  PubMed  PubMed Central  Google Scholar 

  • Upadhyaya DC, Bagri DS, Upadhyaya CP, Kumar A, Thiruvengadam M, Jain SK (2021) Genetic engineering of potato (Solanum tuberosum L.) for enhanced α-tocopherols and abiotic stress tolerance. Physiol Plant 173:116–128

    PubMed  CAS  Google Scholar 

  • Verma SK, Sahu PK, Kumar K, Pal G, Gond SK, Kharwar RN, White JF (2021) Endophyte roles in nutrient acquisition, root system architecture development and oxidative stress tolerance. J Appl Microbiol 131:2161–2177

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Sun R, Tian Y, Guo K, Sun H, Liu X, Chu H, Liu B (2020) Long-term phytoremediation of coastal saline soil reveals plant species-specific patterns of microbial community recruitment. Msystems 5:e00741-e819

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang X, Shao X, Zhang W, Sun T, Ding Y, Lin Z, Li Y (2022) Genus Suaeda: advances in phytology, chemistry, pharmacology and clinical application (1895–2021). Pharmacol Res 179:106203

  • Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T, Bun C, Conrad N, Dietrich EM, Disz T, Gabbard JL (2017) Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 45:535–542

    Article  Google Scholar 

  • Xiong Y-W, Li X-W, Wang T-T, Gong Y, Zhang C-M, Xing K, Qin S (2020) Root exudates-driven rhizosphere recruitment of the plant growth-promoting rhizobacterium Bacillus flexus KLBMP 4941 and its growth-promoting effect on the coastal halophyte Limonium sinense under salt stress. Ecotoxicol Environ Saf 194:110374

    Article  PubMed  CAS  Google Scholar 

  • Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Y, Fang J, Wu X, Dong L (2018) Na+/K+ balance and transport regulatory mechanisms in weedy and cultivated rice (Oryza sativa L.) under salt stress. BMC Plant Biol 18:1–14

    Article  Google Scholar 

  • Zilaie MN, Arani AM, Etesami H, Dinarvand M, Dolati A (2022a) Halotolerant plant growth-promoting rhizobacteria-mediated alleviation of salinity and dust stress and improvement of forage yield in the desert halophyte Seidlitzia rosmarinus. Environ Exp Bot 201:104952

    Article  CAS  Google Scholar 

  • Zilaie MN, Arani AM, Etesami H, Dinarvand M (2022b) Halotolerant rhizobacteria enhance the tolerance of the desert halophyte Nitraria schoberi to salinity and dust pollution by improving its physiological and nutritional status. Appl Soil Ecol 179:104578

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 32200094), Hubei Key Laboratory of Biological Resources Protection and Utilization (Hubei Minzu University) (No. PT012201).

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Peng, M., Jiang, Z., Xiang, Z. et al. Genomic features of a plant growth-promoting endophytic Enterobacter cancerogenus JY65 dominant in microbiota of halophyte Suaeda salsa. Plant Soil 496, 269–287 (2024). https://doi.org/10.1007/s11104-023-06360-5

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