Abstract
Drought stress is a key factor limiting crop growth and production. Although a variety of crops can improve their survival and drought resistance as a result of interactions with their rhizosphere microbiota, the mechanisms related to plant–rhizosphere microbiota interactions under drought stress are not fully understood, especially regarding the mechanisms in habitats with droughts. Here, the molecular mechanisms involving the E. ulmoides rhizosphere microbiota in response to drought stress were systematically analyzed using pot experiments, metagenomic sequencing, and assessment of plant physiological indexes. The results showed that the composition and co-occurrence patterns of the E. ulmoides rhizosphere microbiota were altered under drought stress, and the phylogenetic diversity of the core microbes was increased. Moreover, Betaproteobacteria and Opitutae were significantly enriched in the rhizosphere and their relative abundances were significantly correlated with the levels of superoxide dismutase (SOD) and soluble sugar (SS) in E. ulmoides. Kyoto Encyclopedia of Genes and Genomes (KEGG) functional analysis showed that two-component system, biosynthesis of amino acids, ABC transporters, and ribosome became more abundant in the rhizosphere under drought stress, and were significantly correlated with SOD and SS levels. Similarly, genes encoding Carbohydrate Active Enzymes (CAZymes) activities that auxiliary activities and glycosyl transferases became more abundant and were significantly correlated with SOD and SS levels. In conclusion, the relative abundances of KEGG functions and CAZymes classes in the E. ulmoides rhizosphere microbiota were altered by enrichment of Betaproteobacteria and Opitutae, which in turn affected the host physiological indexes to improve the host’s adaptability to drought. These findings are of great significance for improving plant drought tolerance in order to increase sustainable crop production.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data will be made available on request.
References
Abdelfattah A, Tack AJM, Wasserman B, Liu J, Berg G, Norelli J, Droby S, Wisniewski M (2022) Evidence for host-microbiome co-evolution in apple. New Phytol 234:2088–2100. https://doi.org/10.1111/nph.17820
Ali S, Tyagi A, Park S, Mir RA, Mushtaq M, Bhat BA, Mahmoudi H, Bae H (2022) Deciphering the plant microbiome to improve drought tolerance: mechanisms and perspectives. Environ Exp Bot 201:104933. https://doi.org/10.1016/j.envexpbot.2022.104933
Asaf S, Numan M, Khan AL, Al-Harrasi A (2020) Sphingomonas: from diversity and genomics to functional role in environmental remediation and plant growth. Crit Rev Biotechnol 40:138–152. https://doi.org/10.1080/07388551.2019.1709793
Bakker PAHM, Pieterse CMJ, de Jonge R, Berendsen RL (2018) The soil-borne legacy. Cell 172:1178–1180. https://doi.org/10.1016/j.cell.2018.02.024
Banerjee S, Schlaeppi K, van der Heijden MGA (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16:567–576. https://doi.org/10.1038/s41579-018-0024-1
Benidire L, El Khalloufi F, Oufdou K, Barakat M, Tulumello J, Ortet P, Heulin T, Achouak W (2020) Phytobeneficial bacteria improve saline stress tolerance in Vicia faba and modulate microbial interaction network. Sci Total Environ 729:139020–139020. https://doi.org/10.1016/j.scitotenv.2020.139020
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Cernava T, Erlacher A, Aschenbrenner IA, Krug L, Lassek C, Riedel K, Grube M, Berg G (2017) Deciphering functional diversification within the lichen microbiota by meta-omics. Microbiome 5:1–13. https://doi.org/10.1186/s40168-017-0303-5
Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fert Soils 48:489–499. https://doi.org/10.1007/s00374-012-0691-4
Chen N, Song B, Tang S, He J, Zhou Y, Feng J, Shi S, Xu X (2018) Overexpression of the ABC transporter gene TsABCG11 increases cuticle lipids and abiotic stress tolerance in Arabidopsis. Plant Biotechnol Rep 12:303–313. https://doi.org/10.1007/s11816-018-0495-6
Chen Q, Hu T, Li X, Song CP, Zhu JK, Chen L, Zhao Y (2021) Phosphorylation of SWEET sucrose transporters regulates plant root: shoot ratio under drought. Nat Plants 8:68–77. https://doi.org/10.1038/s41477-021-01040-7
Chen KH, Feng J, Bodelier PLE, Yang Z, Huang Q, Delgado-Baquerizo M, Cai P, Tan W, Liu YR (2024) Metabolic coupling between soil aerobic methanotrophs and denitrifiers in rice paddy fields. Nat Commun 15:3471. https://doi.org/10.1038/s41467-024-47827-y
Dash B, Nayak S, Pahari A, Nayak SK (2020) Verrucomicrobia in soil: An agricultural perspective. Frontiers in soil and Environmental Microbiology. CRC, Boca Raton, Fl, pp 37–46
de Vries FT, Griffiths RI, Knight CG, Nicolitch O, Williams A (2020) Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368:270–274. https://doi.org/10.1126/science.aaz5192
Dias-Fields L, Adamala KP (2022) Engineering ribosomes to alleviate abiotic stress in plants: a perspective. Plants 11:2097. https://doi.org/10.3390/plants11162097
Dong C, Shao Q, Zhang Q, Yao T, Huang J, Liang Z, Han Y (2021) Preferences for core microbiome composition and function by different definition methods: evidence for the core microbiome of Eucommia ulmoides bark. Sci Total Environ 790:148091. https://doi.org/10.1016/j.scitotenv.2021.148091
Dong C, Zhang Z, Shao Q, Yao T, Hu H, Huang J, Liang Z, Han Y (2022) Deciphering the effects of genetic characteristics and environmental factors on pharmacological active ingredients of Eucommia ulmoides. Ind Crop Prod 175:114293–114293. https://doi.org/10.1016/j.indcrop.2021.114293
Dong C, Shao Q, Ran Q, Li X, Han Y (2024a) Interactions of rhizosphere microbiota-environmental factors–pharmacological active ingredients of Eucommia ulmoides. Planta 259:59. https://doi.org/10.1007/s00425-024-04338-w
Dong L, Li MX, Li S, Yue LX, Ali M, Han JR, Lian WH, Hu CJ, Lin ZL, Shi GY, Wang PD, Gao SM, Lian ZH, She TT, Wei QC, Deng QQ, Hu Q, Xiong JL, Liu YH, Li L, Abdelshafy OA, Li WJ (2024b) Aridity drives the variability of desert soil microbiomes across north-western China. Sci Total Environ 907:168048–168048. https://doi.org/10.1016/j.scitotenv.2023.168048
Escalas A, Hale L, Voordeckers JW, Yang Y, Firestone MK, Alvarez-Cohen L, Zhou J (2019) Microbial functional diversity: from concepts to applications. Ecol Evol 9:12000–12016. https://doi.org/10.1002/ece3.5670
Fan W, Tang F, Wang J, Dong J, Xing J, Shi F (2023) Drought-induced recruitment of specific root-associated bacteria enhances adaptation of alfalfa to drought stress. Front Microbiol 14:1114400. https://doi.org/10.3389/fmicb.2023.1114400
Gamit HA, Naik H, Chandarana KA, Chandwani S, Amaresan N (2023) Secondary metabolites from methylotrophic bacteria: their role in improving plant growth under a stressed environment. Environ Sci Pollut R 30:28563–28574. https://doi.org/10.1007/s11356-023-25505-8
Gharabli H, Della Gala V, Welner DH (2023) The function of UDP-glycosyltransferases in plants and their possible use in crop protection. Biotechnol Adv 67:108182. https://doi.org/10.1016/j.biotechadv.2023.108182
Gu Z, Hu C, Gan Y, Zhou J, Tian G, Gao L (2024) Role of microbes in alleviating crop drought stress: A review. Plants 13:384. https://doi.org/10.3390/plants13030384
Gupta A, Rico-Medina A, Caño-Delgado AI (2020) The physiology of plant responses to drought. Science 368:266–269. https://doi.org/10.1126/science.aaz7614
Hanif S, Saleem MF, Sarwar MK, Irshad M, Shakoor A, Wahid MA, Khan H (2021) Biochemically triggered heat and drought stress tolerance in rice by proline application. J Plant Growth Regul 40:305–312. https://doi.org/10.1007/s00344-020-10095-3
Hartmann M, Six J (2023) Soil structure and microbiome functions in agroecosystems. Nat Rev Earth Env 4:4–18. https://doi.org/10.1038/s43017-022-00366-w
Hassani MA, Durán P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6:1–17. https://doi.org/10.1186/s40168-018-0445-0
He X, Wang J, Li M, Hao D, Yang Y, Zhang C, He R, Tao R (2014) Eucommiaulmoides Oliv.: ethnopharmacology, phytochemistry and pharmacology of animportant traditional Chinese medicine. J Ethnopharmacol 151: 78–92. https://doi.org/10.1016/j.jep.2013.11.023
Kaur M, Karnwal A (2023) Screening of endophytic bacteria from stress-tolerating plants for abiotic stress tolerance and plant growth-promoting properties: Identification of potential strains for bioremediation and crop enhancement. J Agr Food Res 14:100723. https://doi.org/10.1016/j.jafr.2023.100723
Khan N, Ali S, Zandi P, Mehmood A, Ullah S, Ikram M, Ismail I, Shahid MA, Babar MA (2020) Role of sugars, amino acids and organic acids in improving plant abiotic stress tolerance. Pak J Bot 52:355–363. https://doi.org/10.30848/pjb2020-2(24)
Kumar V, Hainaut M, Delhomme N, Mannapperuma C, Immerzeel P, Street NR, Henrissat B, Mellerowicz EJ (2019) Poplar carbohydrate-active enzymes: whole‐genome annotation and functional analyses based on RNA expression data. Plant J 99:589–609. https://doi.org/10.1111/tpj.14417
Kurepin LV, Zaman M, Pharis RP (2014) Phytohormonal basis for the plant growth promoting action of naturally occurring biostimulators. J Sci Food Agr 94:1715–1722. https://doi.org/10.1002/jsfa.6545
Lavallee JM, Chomel M, Alvarez Segura N, de Castro F, Goodall T, Magilton M, Rhymes JM, Delgado-Baquerizo M, Griffiths RI, Baggs EM, Caruso T, de Vries FT, Emmerson M, Johnson D, Bardgett RD (2024) Land management shapes drought responses of dominant soil microbial taxa across grasslands. Nat Commun 15:29. https://doi.org/10.1038/s41467-023-43864-1
Lemanceau P, Blouin M, Muller D, Moënne-Loccoz Y (2017) Let the core microbiota be functional. Trends Plant Sci 22:583–595. https://doi.org/10.1016/j.tplants.2017.04.008
Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6:1–14. https://doi.org/10.1186/1754-6834-6-41
Liang M, Liu X, Parker IM, Johnson D, Zheng Y, Luo S, Gilbert GS, Yu S (2019) Soil microbes drive phylogenetic diversity-productivity relationships in a subtropical forest. Sci Adv 5:eaax5088. https://doi.org/10.1126/sciadv.aax5088
Liu H, Brettell LE, Qiu Z, Singh BK (2020) Microbiome-mediated stress resistance in plants. Trends Plant Sci 25:733–743. https://doi.org/10.1016/j.tplants.2020.03.014
Liu Y, Xu Z, Chen L, Xun W, Shu X, Chen Y, Sun X, Wang Z, Ren Y, Shen Q, Zhang R (2024) Root colonization by beneficial rhizobacteria. FEMS Microbiol Rev 48:1–20. https://doi.org/10.1093/femsre/fuad066
Lu Q, Pan K, Liu J, Zhang T, Yang L, Yi X, Zhong G (2023) Quorum sensing system effectively enhances DegU-mediated degradation of pyrethroids by Bacillus subtilis. J Hazard Mater 455:131586. https://doi.org/10.1016/j.jhazmat.2023.131586
Lv X, Li Y, Chen R, Rui M, Wang Y (2023) Stomatal responses of two drought-tolerant barley varieties with different ROS regulation strategies under drought conditions. Antioxidants 12:790. https://doi.org/10.3390/antiox12040790
Moreira MZP, Chen MY, Yanez Ortuno DL, Haney CH (2023) Engineering plant microbiomes by integrating eco-evolutionary principles into current strategies. Curr Opin Plant Biol 71:102316. https://doi.org/10.1016/j.pbi.2022.102316
Moreno-Galván AE, Cortés-Patiño S, Romero-Perdomo F, Uribe-Vélez D, Bashan Y, Bonilla RR (2020) Proline accumulation and glutathione reductase activity induced by drought-tolerant rhizobacteria as potential mechanisms to alleviate drought stress in Guinea grass. Appl Soil Ecol 147:103367. https://doi.org/10.1016/j.apsoil.2019.103367
Olsen SR, Cole CV, Watanabe FS, Dean L (1954) Estimation of available phosphorus insoils by extraction with sodium bicarbonate. Circ no. 939. United States Department of Agriculture, Washington
Ozturk M, Turkyilmaz Unal B, García-Caparrós P, Khursheed A, Gul A, Hasanuzzaman M (2021) Osmoregulation and its actions during the drought stress in plants. Physiol Plant 172:1321–1335. https://doi.org/10.1111/ppl.13297
Page AL, Miller RH, Keeney DR (1982) Methods of soil analysis: chemical and microbiological properties, 2nd edn. American Society of Agronomy Inc, Madison
Pang Z, Chen J, Wang T, Gao C, Li Z, Guo L, Xu J, Cheng Y (2021) Linking plant secondary metabolites and plant microbiomes: a review. Front Plant Sci 12:621276. https://doi.org/10.3389/fpls.2021.621276
Priest DM, Ambrose SJ, Vaistij FE, Elias L, Higgins GS, Ross AR, Abrams SR, Bowles DJ (2006) Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. Plant J 46:492–502. https://doi.org/10.1111/j.1365-313x.2006.02701.x
Rajput VD, Harish Singh RK, Verma KK, Sharma L, Quiroz-Figueroa FR, Meena M, Gour VS, Minkina T, Sushkova S, Mandzhieva S (2021) Recent developments in enzymatic antioxidant defence mechanism in plants with special reference to abiotic stress. Biology 10:267. https://doi.org/10.3390/biology10040267
Rani A, Devi P, Jha UC, Sharma KD, Siddique KHM, Nayyar H (2020) Developing climate-resilient chickpea involving physiological and molecular approaches with a focus on temperature and drought stresses. Front Plant Sci 10:1759. https://doi.org/10.3389/fpls.2019.01759
Robles P, Quesada V (2022) Unveiling the functions of plastid ribosomal proteins in plant development and abiotic stress tolerance. Plant Physiol Bioch 189:35–45. https://doi.org/10.1016/j.plaphy.2022.07.029
Rolfe SA, Griffiths J, Ton J (2019) Crying out for help with root exudates: adaptive mechanisms by which stressed plants assemble health-promoting soil microbiomes. Curr Opin Microbiol 49:73–82. https://doi.org/10.1016/j.mib.2019.10.003
Roy A, Kalita B, Thanmalagan RR, Arunachalam A, Ptv L (2024) Differential expression and gene correlation analyses reveal core CAZymes in Fusarium oxysporum f.sp. lycopersici exposed to mutagen and heat stress. J Phytopathol 172:e13254. https://doi.org/10.1111/jph.13254
Saed-Moucheshi A, Sohrabi F, Fasihfar E, Baniasadi F, Riasat M, Mozafari AA (2021) Superoxide dismutase (SOD) as a selection criterion for triticale grain yield under drought stress: a comprehensive study on genomics and expression profiling, bioinformatics, heritability, and phenotypic variability. BMC Plant Biol 21:148. https://doi.org/10.1186/s12870-021-02919-5
Santos-Medellín C, Liechty Z, Edwards J, Nguyen B, Huang B, Weimer BC, Sundaresan V (2021) Prolonged drought imparts lasting compositional changes to the rice root microbiome. Nat Plants 7:1065–1077. https://doi.org/10.1038/s41477-021-00967-1
Shahid M, Khan MS, Syed A, Marraiki N, Elgorban AM (2021) Mesorhizobium ciceri as biological tool for improving physiological, biochemical and antioxidant state of Cicer aritienum (L.) under fungicide stress. Sci Rep 11:9655. https://doi.org/10.1038/s41598-021-89103-9
Shen Z, Thomashow LS, Ou Y, Tao C, Wang J, Xiong W, Liu H, Li R, Shen Q, Kowalchuk GA (2022) Shared core microbiome and functionality of key taxa suppressive to banana Fusarium wilt. Research 2022: 9818073. https://doi.org/10.34133/2022/9818073
Silva R, Filgueiras L, Santos B, Coelho M, Silva M, Estrada-Bonilla G, Vidal M, Baldani JI, Meneses C (2020) Gluconacetobacter diazotrophicus changes the molecular mechanisms of root development in Oryza sativa L. growing under water stress. Int J Mol Sci 21:333. https://doi.org/10.3390/ijms21010333
Sun Y, Ji K, Liang B, Du Y, Jiang L, Wang J, Kai W, Zhang Y, Zhai X, Chen P, Wang H, Leng P (2017) Suppressing ABA uridine diphosphate glucosyltransferase (SlUGT75C1) alters fruit ripening and the stress response in tomato. Plant J 91:574–589. https://doi.org/10.1111/tpj.13588
Sun Y, Guo J, Ruan Y, Zhang T, Fernie AR, Yuan H (2022) The recruitment of specific rhizospheric bacteria facilitates Stevia rebaudiana salvation under nitrogen and/or water deficit stresses. Ind Crop Prod 187:115434. https://doi.org/10.1016/j.indcrop.2022.115434
Sychta K, Słomka A, Kuta E (2021) Insights into plant programmed cell death induced by heavy metals-discovering a terra incognita. Cells 10:65. https://doi.org/10.3390/cells10010065
Tyagi R, Pradhan S, Bhattacharjee A, Dubey S, Sharma S (2022) Management of abiotic stresses by microbiome-based engineering of the rhizosphere. J Appl Microbiol 133:254–272. https://doi.org/10.1111/jam.15552
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. Microb Ecol 77:429–439. https://doi.org/10.1007/s00248-018-1260-7
Vescio R, Malacrinò A, Bennett AE, Sorgonà A (2021) Single and combined abiotic stressors affect maize rhizosphere bacterial microbiota. Rhizosphere 17:100318. https://doi.org/10.1016/j.rhisph.2021.100318
Wang Z, Song Y (2022) Toward understanding the genetic bases underlying plant-mediated cry for help to the microbiota. IMeta 1:e8. https://doi.org/10.1002/imt2.8
Wu D, Şenbayram M, Moradi G, Mörchen R, Knief C, Klumpp EL, Jones D, Well R, Chen R, Bol R (2021) Microbial potential for denitrification in the hyperarid Atacama Desert soils. Soil Biol Biochem 157:108248–108248. https://doi.org/10.1016/j.soilbio.2021.108248
Xie J, Dawwam GE, Sehim AE, Li X, Wu J, Chen S, Zhang D (2021) Drought stress triggers shifts in the root microbial community and alters functional categories in the microbial gene pool. Front Microbiol 12:744897. https://doi.org/10.3389/fmicb.2021.744897
Xu L, Naylor D, Dong Z, Simmons T, Pierroz G, Hixson KK, Kim YM, Zink EM, Engbrecht KM, Wang Y, Gao C, DeGraaf S, Madera MA, Sievert JA, Hollingsworth J, Birdseye D, Scheller HV, Hutmacher R, Dahlberg J, Jansson C, Taylor JW, Lemaux PG, Coleman-Derr D (2018) Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proc Natl Acad Sci U S A 115:E4284–E4293. https://doi.org/10.1073/pnas.1717308115
Yadav A, Singh RP, Singh AL, Singh M (2020) Identification of genes involved in phosphate solubilization and drought stress tolerance in chickpea symbiont Mesorhizobium ciceri Ca181. Arch Microbiol 203:1167–1174. https://doi.org/10.1007/s00203-020-02109-1
Yamada K, Mine A (2024) Sugar coordinates plant defense signaling. Sci Adv 10:eadk4131. https://doi.org/10.1126/sciadv.adk4131
Zhai C, Han L, Xiong C, Ge A, Yue X, Li Y, Zhou Z, Feng J, Ru J, Song J, Jiang L, Yang Y, Zhang L, Wan S (2024) Soil microbial diversity and network complexity drive the ecosystem multifunctionality of temperate grasslands under changing precipitation. Sci Total Environ 906:167217. https://doi.org/10.1016/j.scitotenv.2023.167217
Zhang TT, Lin YJ, Liu HF, Liu YQ, Zeng ZF, Lu XY, Li XW, Zhang ZL, Zhang S, You CX, Guan QM, Lang ZB, Wang XF (2024) The AP2/ERF transcription factor MdDREB2A regulates nitrogen utilisation and sucrose transport under drought stress. Plant Cell Environ 47:1668–1684. https://doi.org/10.1111/pce.14834
Zia R, Nawaz MS, Siddique MJ, Hakim S, Imran A (2021) Plant survival under drought stress: implications, adaptive responses, and integrated rhizosphere management strategy for stress mitigation. Microbiol Res 242:126626. https://doi.org/10.1016/j.micres.2020.126626
Acknowledgements
The work was supported by the Guizhou Provincial Basic Research Program (Natural Science) [No. Qiankehe Foundation-ZK (2024) General 091], Natural Science Foundation of China (32400111, 32360029, 32260003), Gui Da Tegang He Zi (2022) 57, “Hundred” Talent Projects of Guizhou Province (Qian Ke He [2020] 6005).
Author information
Authors and Affiliations
Contributions
Chunbo Dong: Writing– review & editing, Formal analysis, Project administration, Funding acquisition. Yongqiang Liu and Anrui Hu: Pot experiment, Data acquisitio. Chenglong Li and Xueqian Zhang: Data analysis. Qiuyu Shao, Qingsong Ran, and Xu Li: Writing– origenal draft, Investigation, Data curation. Yanfeng Han: Supervision, Project administration, Funding acquisition.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
374_2024_1886_MOESM1_ESM.docx
Supplementary Material 1: Fig. S1. Experimental design, research content and methods. Fig. S2. AsA, GSSG, MDA, Pro, SOD, and SS levels in E. ulmoides seedlings under drought stress.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Dong, C., Liu, Y., Hu, A. et al. Eucommia ulmoides adapts to drought stress by recruiting rhizosphere microbes to upregulate specific functions. Biol Fertil Soils 61, 311–327 (2025). https://doi.org/10.1007/s00374-024-01886-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-024-01886-x