Microbiome structure and response to watering in rhizosphere of Nitrosalsola vermiculata and surrounding bulk soil

  • Haneen W. ABUAUF Umm Al-Qura University, Department of Biology, Faculty of Applied Science, Makkah (SA)
  • Rewaa S. JALAL University of Jeddah, College of Science, Department of Biology, Jeddah (SA)
  • Ruba A. ASHY University of Jeddah, College of Science, Department of Biology, Jeddah (SA)
  • Ashwag SHAMI Department of Biology, College of Sciences, Princess Nourah bint Abdulrahman University, P.O. Box 84428, Riyadh 11671 (SA)
  • Hanadi M. BAEISSA University of Jeddah, College of Science, Department of Biochemistry, Jeddah (SA)
  • Lina BAZ King AbdulAziz University, Department of Biochemistry, Faculty of Science, Jeddah (SA)
  • Manal A. TASHKANDI University of Jeddah, College of Science, Department of Biochemistry, Jeddah (SA)
  • Aala A. ABULFARAJ Department of Biological Sciences, College of Sciences and Arts, King Abdulaziz University, Rabigh, Saudi Arabia (SA)
Keywords: Alpha and beta indices, drought, operational taxonomic unit (OTU), phylogenetic tree

Abstract

The plant rhizosphere microbiomes were thought to help the plant stands adverse condition. The study aims at deciphering signatures of rhizosphere soil microbiomes of the medicinal plant Nitrosalsola vermiculata and those of the surrounding bulk soil as well as to detect influence of watering in restructuring soil microbes that can improve the plant’s ability to tolerate drought stress. Amplicon sequencing of partial 16S rRNA gene indicated that alpha diversity indices are higher in rhizosphere than in bulk soils, while no distinctive differences were observed due to the watering. Relative abundance of phylum Cyanobacteria and its descendent unidentified genus is the highest among phyla and genera of bulk soil. Relative abundance of phyla Euryarchaeota, Chloroflexi, Actinobacteria, Proteobacteria, Bacteroidetes, Firmicutes, Acidobacteria and Gemmatimonadetes as well as genera Bacillus, Ammoniphilus, Sphingomonas, Microvirga, Pontibacter, Adhaeribacter and Arthrobacter was significantly higher in rhizosphere soil. The latter taxa were reported to act as plant growth-promoting bacteria (PGPB) through symbiotic associations. We speculate that relative abundance and mutual dominance of these taxa in rhizosphere of N. vermiculata were due to the intensity and type of plant root exudates. Other factors include soil pH where microbes favoring high soil pH can show better growth in rhizosphere soil. Also, co-existence of phyla that promote sustainability of cohabiting phyla in the rhizosphere and have high synergism prevalence in biofilm formation can be one extra factor. Quorum sensing (QS) also mediates bacterial population density in a given environment and elicit specific plant responses. The low abundance of Cyanobacteria in rhizosphere soil can be due to the inhibitory effect of highly abundant members of Firmicutes, especially those of genus Bacillus. The latter conclusion was confirmed by the occurrence of high expression rate of comQ gene triggering QS in genus Bacillus. Highly abundant microbes whose abundance was not changed due to watering are phyla Firmicutes, Proteobacteria, Chloroflexi and Cyanobacteria and their descendent genera Bacillus, Ammoniphilus, Sphingomonas, Microvirga and unidentified genus of Cyanobacteria. We speculate that non-responsive taxa to watering were drought tolerant and can help plants stand adverse conditions of water scarce. In conclusion, insights on the factors involved in shaping microbiome signatures and those eliciting differential plant responses to drought stress are raised and warrant further investigations.

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References

Afonso AC, Gomes IB, Saavedra MJ, Giaouris E, Simoes LC, Simoes M (2021). Bacterial coaggregation in aquatic systems. Water Research 196:117037. https://doi.org/10.1016/j.watres.2021.117037

Al-Eisawi DM, Al-Ruzayza S (2015). The flora of holy Mecca district, Saudi Arabia. International Journal of Biodiversity and Conservation 7:173-189. https://doi.org/10.5897/IJBC2014.0773

Al-Tabini R, Al-Khalidi K, Al-Shudiefat M (2012). Livestock, medicinal plants and rangeland viability in Jordan’s Badia: Through the lens of traditional and local knowledge. Pastoralism: Research, Policy and Practice 2:1-16. https://doi.org/10.1186/2041-7136-2-4

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990). Basic local alignment search tool. Journal of Molecular Biology 215:403-410. https://doi.org/10.1016/S0022-2836(05)80360-2

Bahieldin A, Atef A, Sabir JS, Gadalla NO, Edris S, Alzohairy AM, … Jansen RK (2015). RNA-Seq analysis of the wild barley (H. spontaneum) leaf transcriptome under salt stress. Comptes Rendus Biologies 338:285-297. https://doi.org/10.1016/j.crvi.2015.03.010

Barnard RL, Osborne CA, Firestone MK (2013). Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. The ISME Journal 7:2229-2241. https://doi.org/10.1038/ismej.2013.104

Batool T, Ali S, Seleiman MF, Naveed NH, Ali A, Ahmed K, … Mubushar M (2020). Plant growth promoting rhizobacteria alleviates drought stress in potato in response to suppressive oxidative stress and antioxidant enzymes activities. Scientific Reports 10:16975. https://doi.org/10.1038/s41598-020-73489-z

Berg G, Grube M, Schloter M, Smalla K (2014). Unraveling the plant microbiome: looking back and future perspectives. Frontiers in Microbiology 5:148. https://doi.org/10.3389/fmicb.2014.00148

Bergman B, Rai A, Rasmussen U (2007). Cyanobacterial associations. In: Elmerich C, Newton WE (Eds). Associative and Endophytic Nitrogen-Fixing Bacteria and Cyanobacterial Associations. Springer, pp 257-301.

Bokhari A, Essack M, Lafi FF, Andres-Barrao C, Jalal R, Alamoudi S, Razali R, … Siddique S (2019). Bioprospecting desert plant Bacillus endophytic strains for their potential to enhance plant stress tolerance. Scientific reports 9:1-13. https://doi.org/10.1038/s41598-019-54685-y

Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013). Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature Methods 10:57-59. https://doi.org/10.1038/nmeth.2276

Breitkreuz C, Herzig L, Buscot F, Reitz T, Tarkka M (2021). Interactions between soil properties, agricultural management and cultivar type drive structural and functional adaptations of the wheat rhizosphere microbiome to drought. Environmental Microbiology 23:5866-5882. https://doi.org/10.1111/1462-2920.15607

Bu X, Gu X, Zhou X, Zhang M, Guo Z, Zhang J, … Wang X (2018). Extreme drought slightly decreased soil labile organic C and N contents and altered microbial community structure in a subtropical evergreen forest. Forest Ecology and Management 429:18-27. https://doi.org/10.1016/j.foreco.2018.06.036

Bulgarelli D, Garrido-Oter R, Munch PC, Weiman A, Droge J, Pan Y, … Schulze-Lefert P (2015). Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392-403. https://doi.org/10.1016/j.chom.2015.01.011

Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, … Gordon JI (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7:335-336. https://doi.org/10.1038/nmeth.f.303

Chodak M, Gołębiewski M, Morawska-Płoskonka J, Kuduk K, Niklińska M (2015). Soil chemical properties affect the reaction of forest soil bacteria to drought and rewetting stress. Annals of Microbiology 65:1627-1637. https://doi.org/10.1007/s13213-014-1002-0

Chukwuneme CF, Babalola OO, Kutu FR, Ojuederie OB (2020). Characterization of actinomycetes isolates for plant growth promoting traits and their effects on drought tolerance in maize. Journal of Plant Interactions 15:93-105. https://doi.org/10.1080/17429145.2020.1752833

Cuddy WS, Neilan BA, Gehringer MM (2012). Comparative analysis of cyanobacteria in the rhizosphere and as endosymbionts of cycads in drought-affected soils. FEMS Microbiology Ecology 80:204-215. https://doi.org/10.1111/j.1574-6941.2011.01288.x

Dai L, Zhang G, Yu Z, Ding H, Xu Y, Zhang Z (2019). Effect of drought stress and developmental stages on microbial community structure and diversity in peanut rhizosphere soil. International Journal of Molecular Sciences 20:2265. https://doi.org/10.3390/ijms20092265

Disi AM, Damhoureyeh SA, Al-Khader IA, Al-Jbour S (2004). The Badia of Jordan: Biodiversity, threats and conservation. Annals of Arid Zone 43:293.

Edgar RC (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32:1792-1797. https://doi.org/10.1093/nar/gkh340

Edgar RC (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10:996-998. https://doi.org/10.1038/nmeth.2604

Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194-2200. https://doi.org/10.1093/bioinformatics/btr381

Eichorst SA, Trojan D, Roux S, Herbold C, Rattei T, Woebken D (2018). Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments. Environmental Microbiology 20:1041-1063. https://doi.org/10.1111/1462-2920.14043

Fan D, Han J, Chen Y, Zhu Y, Li P (2018). Hormetic effects of Cd on alkaline phosphatase in soils across particle–size fractions in a typical coastal wetland. Science of the Total Environment 613:792-797. http://dx.doi.org/10.1016/j.scitotenv.2017.09.089

Feodorova T (2015). New nomenclatural combinations in Nitrosalsola (Chenopodiaceae). Ukrainian Botanical Journal 72:442-445. https://doi.org/10.15407/ukrbotj72.05.442

Geng L-L, Shao G-X, Raymond B, Wang M-L, Sun X-X, Shu C-L, Zhang J (2018). Subterranean infestation by Holotrichia parallela larvae is associated with changes in the peanut (Arachis hypogaea L.) rhizosphere microbiome. Microbiological Research 211:13-20. https://doi.org/10.1016/j.micres.2018.02.008

Glick BR (2012). Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo) 2012:963401. https://doi.org/10.6064/2012/963401

Gumiere T, Gumiere SJ, Matteau J-P, Constant P, Létourneau G, Rousseau AN (2019). Soil bacterial community associated with high potato production and minimal water use. Frontiers in Environmental Science 6:161. https://doi.org/10.3389/fenvs.2018.00161

Herrera N, Echeverri F (2021). Evidence of quorum sensing in cyanobacteria by homoserine lactones: The Origin of Blooms Water 13:1831. https://doi.org/10.3390/w13131831

Hurt RA, Qiu X, Wu L, Roh Y, Palumbo AV, Tiedje JM, Zhou J (2001). Simultaneous recovery of RNA and DNA from soils and sediments. Applied and Environmental Microbiology 67:4495-4503. https://doi.org/10.1128/AEM.67.10.4495-4503.2001

Iverson V, Morris RM, Frazar CD, Berthiaume CT, Morales RL, Armbrust EV (2012). Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science 335:587-590. https://doi.org/10.1126/science.1212665

Jang SW, Yoou MH, Hong WJ, Kim YJ, Lee EJ, Jung KH (2020). Re-analysis of 16S amplicon sequencing data reveals soil microbial population shifts in rice fields under drought condition. Rice (N Y) 13:44. https://doi.org/10.1186/s12284-020-00403-6

Kalam S, Basu A, Ahmad I, Sayyed R, El Enshasy HA, Dailin DJ, Suriani N (2020). Recent understanding of soil Acidobacteria and their ecological significance: A critical review. Frontiers in Microbiology 11:2712. https://doi.org/10.3389/fmicb.2020.580024

Kampmann K, Ratering S, Kramer I, Schmidt M, Zerr W, Schnell S (2012). Unexpected stability of Bacteroidetes and Firmicutes communities in laboratory biogas reactors fed with different defined substrates. Applied and Environmental Microbiology 78:2106-2119. https://doi.org/10.1128/AEM.06394-11

Lazar V, Holban AM, Curutiu C, Chifiriuc MC (2021). Modulation of quorum sensing and biofilms in less investigated gram-negative ESKAPE pathogens. Frontiers in Microbiology 12:676510. https://doi.org/10.3389/fmicb.2021.676510

Li B, Zhang X, Guo F, Wu W, Zhang T (2013). Characterization of tetracycline resistant bacterial community in saline activated sludge using batch stress incubation with high-throughput sequencing analysis. Water Research 47:4207-4216. https://doi.org/10.1016/j.watres.2013.04.021

Liberton M, Page LE, O'Dell WB, O'Neill H, Mamontov E, Urban VS, Pakrasi HB (2013). Organization and flexibility of cyanobacterial thylakoid membranes examined by neutron scattering. Journal of Biological Chemistry 288:3632-3640. https://doi.org/10.1074/jbc.M112.416933

Liesack W, Schnell S, Revsbech NP (2000). Microbiology of flooded rice paddies. FEMS Microbiology Reviews 24:625-645. https://doi.org/10.1111/j.1574-6976.2000.tb00563.x

Lindblad P, Atkins CA, Pate JS (1991). N2-Fixation by freshly isolated Nostoc from coralloid roots of the cycad Macrozamia riedlei (Fisch. ex Gaud.) Gardn. Plant Physiology 95:753-759. https://doi.org/10.1104/pp.95.3.753

Lopes LD, Hao J, Schachtman DP (2021). Alkaline soil pH affects bulk soil, rhizosphere and root endosphere microbiomes of plants growing in a Sandhills ecosystem. FEMS Microbiology Ecology 97:028. https://doi.org/10.1093/femsec/fiab028

Lozupone C, Knight R (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Applied and Environmental Microbiology 71:8228-8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005

Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011). UniFrac: an effective distance metric for microbial community comparison. The ISME Journal 5:169-172. https://doi.org/10.1038/ismej.2010.133

Lozupone CA, Hamady M, Kelley ST, Knight R (2007). Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Applied and Environmental Microbiology 73:1576-1585. https://doi.org/10.1128/AEM.01996-06

Lucy M, Reed E, Glick BR (2004). Applications of free-living plant growth-promoting rhizobacteria. Antonie van Leeuwenhoek 86:1-25. https://doi.org/10.1023/B:ANTO.0000024903.10757.6e

Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, … Del Rio TG (2012). Defining the core Arabidopsis thaliana root microbiome. Nature 488:86-90. https://doi.org/10.1038/nature11237

Lundberg DS, Yourstone S, Mieczkowski P, Jones CD, Dangl JL (2013). Practical innovations for high-throughput amplicon sequencing. Nature Methods 10:999-1002. https://doi.org/10.1038/nmeth.2634

Luo Y, Wang F, Huang Y, Zhou M, Gao J, Yan T, … An L (2019). Sphingomonas sp. Cra20 increases plant growth rate and alters rhizosphere microbial community structure of Arabidopsis thaliana under drought stress. Frontiers in Microbiology 10:1221. https://doi.org/10.3389/fmicb.2019.01221

Luo Y, Zhou M, Zhao Q, Wang F, Gao J, Sheng H, An L (2020). Complete genome sequence of Sphingomonas sp. Cra20, a drought resistant and plant growth promoting rhizobacteria. Genomics 112:3648-3657. https://doi.org/10.1016/j.ygeno.2020.04.013

Ma H-k, Pineda A, Hannula SE, Kielak AM, Setyarini SN, Bezemer TM (2020). Steering root microbiomes of a commercial horticultural crop with plant-soil feedbacks. Applied Soil Ecology 150:103468. https://doi.org/10.1016/j.apsoil.2019.103468

Magoč T, Salzberg SL (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957-2963. https://doi.org/10.1093/bioinformatics/btr507

McLean E (1983). Soil pH and lime requirement. Methods of soil analysis: Part 2. Chemical and Microbiological Properties 9:199-224. https://doi.org/10.2134/agronmonogr9.2.2ed.c12

Miller MB, Bassler BL (2001). Quorum sensing in bacteria. Annual Review of Microbiology 55:165-199. https://doi.org/10.1146/annurev.micro.55.1.165

Miransari M (2011). Soil microbes and plant fertilization. Applied Microbiology and Biotechnology 92:875-885. https://doi.org/10.1007/s00253-011-3521-y

Na X, Cao X, Ma C, Ma S, Xu P, Liu S, … Qiao Z (2019). Plant stage, not drought stress, determines the effect of cultivars on bacterial community diversity in the rhizosphere of broomcorn millet (Panicum miliaceum L.). Frontiers in Microbiology 10:828. https://doi.org/10.3389/fmicb.2019.00828

Nadal-Sala D, Grote R, Birami B, Knuver T, Rehschuh R, Schwarz S, Ruehr NK (2021). Leaf shedding and non-stomatal limitations of photosynthesis mitigate hydraulic conductance losses in scots pine saplings during severe drought stress. Frontiers in Plant Science 12:715127. https://doi.org/10.3389/fpls.2021.715127

Naylor D, DeGraaf S, Purdom E, Coleman-Derr D (2017). Drought and host selection influence bacterial community dynamics in the grass root microbiome. The ISME Journal 11:2691-2704. https://doi.org/10.1038/ismej.2017.118

Ng WL, Bassler BL (2009). Bacterial quorum-sensing network architectures. Annual Review of Genetics 43:197-222. https://doi.org/10.1146/annurev-genet-102108-134304

Nilsson M, Rasmussen U, Bergman B (2005). Competition among symbiotic cyanobacterial Nostoc strains forming artificial associations with rice (Oryza sativa). FEMS Microbiology Letters 245:139-144. https://doi.org/10.1016/j.femsle.2005.03.010

Passari AK, Mishra VK, Saikia R, Gupta VK, Singh BP (2015). Isolation, abundance and phylogenetic affiliation of endophytic actinomycetes associated with medicinal plants and screening for their in vitro antimicrobial biosynthetic potential. Frontiers in Microbiology 6:273. https://doi.org/10.3389/fmicb.2015.00273

Potts M (1994). Desiccation tolerance of prokaryotes. Microbiological Reviews 58:755-805. https://doi.org/10.1128/mr.58.4.755-805.1994

Prasanna R, Jaiswal P, Nayak S, Sood A, Kaushik BD (2009). Cyanobacterial diversity in the rhizosphere of rice and its ecological significance. Indian Journal of Microbiology 49:89-97. https://doi.org/10.1007/s12088-009-0009-x

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41:D590-D596. https://doi.org/10.1093/nar/gks1219

Ramadan AM, Nazar MA, Gadallah NO (2021). Metagenomic analysis of rhizosphere bacteria in desert plant Calotropis procera. Geomicrobiology Journal 38:375-383. https://doi.org/10.1080/01490451.2020.1860166

Ranjan K, Priya H, Ramakrishnan B, Prasanna R, Venkatachalam S, Thapa S, … Shivay YS (2016). Cyanobacterial inoculation modifies the rhizosphere microbiome of rice planted to a tropical alluvial soil. Applied Soil Ecology 108:195-203. https://doi.org/10.1016/j.apsoil.2016.08.010

Ren D, Madsen JS, Sørensen SJ, Burmølle M (2015). High prevalence of biofilm synergy among bacterial soil isolates in cocultures indicates bacterial interspecific cooperation. The ISME Journal 9:81-89. https://doi.org/10.1038/ismej.2014.96

Rutherford ST, Bassler BL (2012). Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med 2, a012427. https://doi.org/10.1101/cshperspect.a012427

Santos-Medellín C, Edwards J, Liechty Z, Nguyen B, Sundaresan V (2017). Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes. mBio 8:e00764-17. https://doi.org/10.1128/mBio.00764-17

Sathya A, Vijayabharathi R, Gopalakrishnan S (2017). Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes. 3 Biotech 7:1-10. https://doi.org/10.1007/s13205-017-0736-3

Seleiman MF, Al-Suhaibani N, Ali N, Akmal M, Alotaibi M, Refay Y, … Battaglia ML (2021). Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants (Basel) 10:259. https://doi.org/10.3390/plants10020259

Sinha RP, Häder D-P (2008). UV-protectants in cyanobacteria. Plant Science 174:278-289. https://doi.org/10.1016/j.plantsci.2007.12.004

Stanley NR, Lazazzera BA (2005). Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly‐γ‐DL‐glutamic acid production and biofilm formation. Molecular Microbiology 57:1143-1158. https://doi.org/10.1111/j.1365-2958.2005.04746.x

Stevens MR, Luo TL, Vornhagen J, Jakubovics NS, Gilsdorf JR, Marrs CF, … Rickard AH (2015). Coaggregation occurs between microorganisms isolated from different environments. FEMS Microbiology Ecology 91:fiv123. https://doi.org/10.1093/femsec/fiv123

Tank M, Bryant DA (2015). Nutrient requirements and growth physiology of the photoheterotrophic Acidobacterium, Chloracidobacterium thermophilum. Frontiers in Microbiology 6:226. https://doi.org/10.3389/fmicb.2015.00226

Timm CM, Carter KR, Carrell AA, Jun SR, Jawdy SS, Velez JM, … Weston DJ (2018). Abiotic stresses shift belowground Populus-associated bacteria toward a core stress microbiome. mSystems 3:e00070-00017. https://doi.org/10.1128/mSystems.00070-17

Ullah A, Akbar A, Luo Q, Khan AH, Manghwar H, Shaban M, Yang X (2019). Microbiome diversity in cotton rhizosphere under normal and drought conditions. Microbial Ecology 77:429-439. https://doi.org/10.1007/s00248-018-1260-7

Wang F-H, Qiao M, Chen Z, Su J-Q, Zhu Y-G (2015). Antibiotic resistance genes in manure-amended soil and vegetables at harvest. Journal of Hazardous Materials 299:215-221. https://doi.org/10.1016/j.jhazmat.2015.05.028

Wang R, Zhang H, Sun L, Qi G, Chen S, Zhao X (2017). Microbial community composition is related to soil biological and chemical properties and bacterial wilt outbreak. Scientific Reports 7:1-10. https://doi.org/10.1038/s41598-017-00472-6

Wei Z, Hu X, Li X, Zhang Y, Jiang L, Li J, … Liao X (2017). The rhizospheric microbial community structure and diversity of deciduous and evergreen forests in Taihu Lake area, China. PLoS One 12:e0174411. https://doi.org/10.1371/journal.pone.0174411

Williams P, Camara M (2009). Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Current Opinion in Microbiology 12:182-191. https://doi.org/10.1016/j.mib.2009.01.005

Wu S, Wu Y, Cao B, Huang Q, Cai P (2021). An invisible workforce in soil: The neglected role of soil biofilms in conjugative transfer of antibiotic resistance genes. Critical Reviews in Environmental Science and Technology 2012:1-29. https://doi.org/10.1080/10643389.2021.1892015

Xu L, Naylor D, Dong Z, Simmons T, Pierroz G, Hixson KK, … Wang Y (2018). Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proceedings of the National Academy of Sciences 115:E4284-E4293. https://doi.org/10.1073/pnas.1717308115

Yadav AN, Verma P, Kumar S, Kumar V, Kumar M, Sugitha TCK, … Dhaliwal HS (2018). Actinobacteria from rhizosphere: molecular diversity, distributions, and potential biotechnological applications. In: Gupta V (Ed). New and Future Developments in Microbial Biotechnology and Bioengineering. Elsevier, pp 13-41.

Zhang R, Chen L, Niu Z, Song S, Zhao Y (2019). Water stress affects the frequency of Firmicutes, Clostridiales and Lysobacter in rhizosphere soils of greenhouse grape. Agricultural Water Management 226:105776. https://doi.org/10.1016/j.agwat.2019.105776

Zhou C, Ma Z, Zhu L, Xiao X, Xie Y, Zhu J, Wang J (2016). Rhizobacterial strain Bacillus megaterium BOFC15 induces cellular polyamine changes that improve plant growth and drought resistance. International Journal of Molecular Sciences 17:976. https://doi.org/10.3390/ijms17060976

Zuo J, Zu M, Liu L, Song X, Yuan Y (2021). Composition and diversity of bacterial communities in the rhizosphere of the Chinese medicinal herb Dendrobium. BMC Plant Biology 21:1-13. https://doi.org/10.1186/s12870-021-02893-y

Published
2022-02-09
How to Cite
ABUAUF, H. W., JALAL, R. S., ASHY, R. A., SHAMI, A., BAEISSA, H. M., BAZ, L., TASHKANDI, M. A., & ABULFARAJ, A. A. (2022). Microbiome structure and response to watering in rhizosphere of Nitrosalsola vermiculata and surrounding bulk soil. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 50(1), 12567. https://doi.org/10.15835/nbha50112567
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Research Articles
CITATION
DOI: 10.15835/nbha50112567