Growth-promoting effect of Enterobacter mori on Reaumuria songarica seedlings under salt stress and its rhizosphere mechanism

doi:10.11686/cyxb2025392

Abstract

Abstract:

In this study， we investigated the effects of plant growth-promoting rhizobacteria （PGPR） on the growth and rhizosphere soil of the desert plant Reaumuria songarica under salt stress. Seedlings of R. songarica were inoculated with the PGPR Enterobacter mori P4 and subjected to 400 mmol·L^-1 NaCl stress， and seedling growth and physiological indicators， as well as soil characteristics and phosphorus functional gene abundance， were determined. The main results were as follows： 1） Under salt stress， the R. songarica seedlings inoculated with P4 showed significantly increased total root length and seedling biomass， compared with those in the control （P<0.05）. Specifically， the group inoculated with P4 showed a significant increase in total root length by 16.5%， as well as increased root dry weight， stem dry weight， and leaf dry weight （by 74.19%， 160.71%， and 92.54%， respectively）. 2） Under salt stress， the seedlings inoculated with P4 showed significantly increased soluble sugar and soluble protein contents （by 64.30% and 18.63%， respectively）， significantly lower malondialdehyde content （by 25.41%）， and decreased proline content （by 3.72%）， compared with the control group. 3） Under salt stress， the activities of sucrase and phosphatase were significantly higher （by 89.64% and 51.06%， respectively）， and the activities of amylase， urease and catalase were significantly lower （by 27.90%， 43.87%， and 3.03% respectively）， in the P4-inoculated seedlings than in the control group. 4） The transcript levels of phosphorus cycle functional genes （gcd， pqqC， ppx， phoD， and phoX） were significantly lower in the rhizosphere soil of the control group than in that of the P4-inoculated seedlings， indicating that P4 can significantly increase the transcript abundance of these functional genes. In summary， P4 stimulates soil microorganisms to synthesize enzymes and increase the expression of genes in the phosphorus cycle， and promotes the accumulation of osmotic adjustment substances in R. songarica， allowing it to maintain cell turgor and enhance its salt tolerance.

Key words: Reaumuria songarica, salt stress, Enterobacter mori, phosphorus functional gene, rhizosphere soil

Kai-xin LOU, Pei-fang CHONG, Xin-guang BAO, Jin-ting XIAO, Jia-li YANG. Growth-promoting effect of Enterobacter mori on Reaumuria songarica seedlings under salt stress and its rhizosphere mechanism[J]. Acta Prataculturae Sinica, 2026, 35(9): 87-99.

Figures/Tables 7

Table 1 Effect of inoculation of E. mori P4 on the biomass of R. songarica seedlings （g·plant-1）

处理 Treatment	叶鲜重 Leaf fresh weight	茎鲜重 Stem fresh weight	根鲜重 Root fresh weight	叶干重 Leaf dry weight	茎干重 Stem dry weight	根干重 Root dry weight
CK	3.26±0.25c	1.60±0.13b	1.34±0.06bc	1.09±0.24b	0.72±0.06b	0.25±0.02b
P4	6.26±0.11a	2.07±0.07a	2.22±0.28a	1.95±0.08a	0.93±0.03a	0.59±0.03a
S	1.44±0.19d	0.57±0.13c	0.76±0.19c	0.67±0.08c	0.28±0.06c	0.31±0.05b
P4+S	4.04±0.19b	1.56±0.07b	1.87±0.13ab	1.29±0.13b	0.73±0.02b	0.54±0.04a

Fig.1 Effect of inoculation of E. mori P4 on the plant height and total root length of R. songarica seedlings

Fig.2 Effect of inoculation of E. mori P4 on the physical and chemical properties of rhizosphere soil of R. songarica seedlings

Fig.3 Effect of inoculation of E. mori P4 on the enzyme activity of rhizosphere soil of R. songarica seedlings

Fig.4 Effect of inoculation of E. mori P4 on the osmotic regulatory substances and malondialdehyde content in leaves of R. songarica seedlings

Fig.5 Effect of inoculation of E.mori P4 on the abundance of phosphorus cycling related functional genes

Fig.6 Effect of inoculation of E. mori P4 under salt stress on the correlation of multiple indicators of R. songarica seedlings system

References 59

[1]	Food and Agriculture Organization of the United Nations （FAO）. Global map of salt-affected soils. （2021-10-21）［2025-09-20］. https：//openknowledge.fao.org/handle/20.500.14283/cb7247en.
[2]	Yang J S， Yao R J， Wang X P， et al. Research on salt-affected soils in China： History， status quo and prospect. Acta Pedologica Sinica， 2022， 59（1）： 10-27.
	杨劲松，姚荣江，王相平，等. 中国盐渍土研究：历程、现状与展望. 土壤学报， 2022， 59（1）： 10-27.
[3]	Wang Z Q， Liu F T. Saline soil in China. Beijing： Science Press， 1993.
	王遵亲，刘福涛. 中国盐渍土. 北京：科学出版社， 1993.
[4]	Munns R， Tester M. Mechanisms of salinity tolerance. Annual Review of Plant Biology， 2008， 59： 651-681.
[5]	Yu Z R， Wang J W. Land salinization in China and the prevention countermeasures. Journal of Ecology and Rural Environment， 1997， 13（3）： 1-5.
	宇振荣，王建武. 中国土地盐碱化及其防治对策研究. 生态与农村环境学报， 1997， 13（3）： 1-5.
[6]	Qadir M， Quillérou E， Nangia V， et al. Economics of salt-induced land degradation and restoration. Natural Resources Forum， 2014， 38（4）： 282-295.
[7]	Glick B R. Plant growth-promoting bacteria： mechanisms and applications. Scientifica， 2012（1）： 963401.
[8]	Bianco C， Defez R. Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. Journal of Experimental Botany， 2009， 60（11）： 3097-3107.
[9]	Vessey J K. Plant growth promoting rhizobacteria as biofertilizers. Plant and Soil， 2003， 255： 571-586.
[10]	Egamberdieva D， Kucharova Z. Selection for root colonising bacteria stimulating wheat growth in saline soils. Biology and Fertility of Soils， 2009， 45（6）： 563-571.
[11]	Mukherjee S， Sen S K. Exploration of novel rhizospheric yeast isolate as fertilizing soil inoculant for improvement of maize cultivation. Journal of the Science of Food and Agriculture， 2015， 95（7）： 1491-1499.
[12]	Amri M， Rjeibi M R， Gatrouni M， et al. Isolation， identification， and characterization of phosphate-solubilizing bacteria from Tunisian soils. Microorganisms， 2023， 11（3）： 783.
[13]	Afzal A， Khan M Y， Zahir Z A， et al. Plant growth-promoting bacterial consortia improved the physiology and growth of maize by regulating osmolytes and antioxidants balance under salt-affected field conditions. Heliyon， 2023， 9（7）： e17816.
[14]	Batool T， Ali S， Seleiman M F， et al. Plant growth promoting rhizobacteria alleviates drought stress in potato in response to suppressive oxidative stress and antioxidant enzymes activities. Scientific Reports， 2020， 10（1）： 16975.
[15]	Neshat M， Abbasi A， Hosseinzadeh A， et al. Plant growth promoting bacteria （PGPR） induce antioxidant tolerance against salinity stress through biochemical and physiological mechanisms. Physiology and Molecular Biology of Plants， 2022， 28（2）： 347-361.
[16]	Hidri R， Mahmoud O M B， Zorrig W， et al. Plant growth-promoting rhizobacteria alleviate high salinity impact on the halophyte Suaeda fruticosa by modulating antioxidant defense and soil biological activity. Frontiers in Plant Science， 2022， 13： 821475.
[17]	Ning Z， Lin K， Gao M， et al. Mitigation of salt stress in rice by the halotolerant plant growth-promoting bacterium Enterobacter asburiae D2. Journal of Xenobiotics， 2024， 14（1）： 333-349.
[18]	Ma J Y， Chen T， Qiang W Y， et al. Correlations between foliar stable carbon isotope composition and environmental factors in desert plant Reaumuria soongorica （Pall.） Maxim. Journal of Integrative Plant Biology， 2005， 47（9）： 1065-1073.
[19]	Yan Y， Guo Q， Dang X H， et al. Comparative study on sand-blocking ability of Tetraena mongolica and Reaumuria soongorica shrubs in the West Ordos area. Bulletin of Soil and Water Conservation， 2024， 44（2）： 137-145， 154.
	闫宇，郭强，党晓宏，等. 西鄂尔多斯地区四合木与红砂灌丛的阻沙能力对比研究. 水土保持通报， 2024， 44（2）： 137-145， 154.
[20]	Zhao X， Yang X J， Shi Y， et al. Ion absorption and distribution of symbiotic Reaumuria soongorica and Salsola passerina seedlings under NaCl stress. Acta Ecologica Sinica， 2014， 34（4）： 963-972.
	赵昕，杨小菊，石勇，等. 盐胁迫下荒漠共生植物红砂与珍珠的根茎叶中离子吸收与分配特征. 生态学报， 2014， 34（4）： 963-972.
[21]	Tan H J， Li X R， Zhao X， et al. Study on mechanisms of osmo regulation of Reaumuria soongorica callus in adapting to salt stress. Journal of Desert Research， 2011， 31（5）： 1119-1123.
	谭会娟，李新荣，赵昕，等. 红砂愈伤组织适应盐胁迫的渗透调节机制研究. 中国沙漠， 2011， 31（5）： 1119-1123.
[22]	Li N N， Du C， Ma B J， et al. Functional analysis of ion transport properties and salt tolerance mechanisms of RtHKT1 from the recretohalophyte Reaumuria trigyna. Plant and Cell Physiology， 2019， 60（1）： 85-106.
[23]	Wang X Y， Bao X G， Zhang F， et al. Characteristics of bacterial community and soil enzyme activity in rhizosphere. Acta Agrestia Sinica， 2024， 32（12）： 3764-3773.
	王雪莹，包新光，张峰，等. 荒漠植物红砂根际土壤细菌群落特征及土壤酶活性研究. 草地学报， 2024， 32（12）： 3764-3773.
[24]	Zhang F， Chong P F， Bao X G， et al. Isolation and identification of four strains of Reaumuria soongorica root zone nitrogen fixing bacteria and their role in seedling growth promotion. Acta Prataculturae Sinica， 2025， 34（3）： 144-153.
	张峰，种培芳，包新光，等. 4株红砂根际固氮菌分离鉴定及对幼苗促生作用的研究. 草业学报， 2025， 34（3）： 144-153.
[25]	Chen J T， Aroca R， Romano D. Molecular aspects of plant salinity stress and tolerance. International Journal of Molecular Sciences， 2021， 22（9）： 4918.
[26]	Yan S， Chong P F， Zhao M. Effect of salt stress on the photosynthetic characteristics and endogenous hormones， and： A comprehensive evaluation of salt tolerance in Reaumuria soongorica seedlings. Plant Signaling & Behavior， 2022， 17（1）： 2031782.
[27]	Ma Q， Su S P， Li Y， et al. Effects of abscisic acid on Reaumuria soongorica seed germination under NaCl stress. Pratacultural Science， 2023， 40（4）： 925-934.
	马强，苏世平，李毅，等. 脱落酸对NaCl胁迫下红砂种子萌发的影响. 草业科学， 2023， 40（4）： 925-934.
[28]	Li H S. Principles and techniques of plant physiological biochemical experiment. Beijing： Higher Education Press， 2000.
	李合生. 植物生理生化实验原理和技术. 北京：高等教育出版社， 2000.
[29]	Bao S D. Soil and agricultural chemistry analysis. Beijing： China Agriculture Press， 2000： 30-76.
	鲍士旦. 土壤农化分析. 北京：中国农业出版社， 2000： 30-76.
[30]	Guan S Y. Soil enzymes and their research methods. Beijing： China Agriculture Press， 1986.
	关松荫. 土壤酶及其研究法. 北京：中国农业出版社， 1986.
[31]	Zheng B X， Zhu Y G， Sardans J， et al. QMEC： A tool for high-throughput quantitative assessment of microbial functional potential in C， N， P， and S biogeochemical cycling. Science China Life Sciences， 2018， 61（12）： 1451-1462.
[32]	Livak K J， Schmittgen T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2^-ΔΔCTmethod. Methods， 2001， 25（4）： 402-408.
[33]	Li J. Screening of plant growth promoting and salt tolerant bacteria from three desert halophytes. Kashi： Kashi University， 2023.
	李静. 三种荒漠盐生植物促生菌筛选及耐盐促生效果评价. 喀什：喀什大学， 2023.
[34]	Glick B R. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiological Research， 2014， 169（1）： 30-39.
[35]	Peng M. Isolation of Enterobacter cancerogenus JY65 and its molecular mechanism of alleviating NaCl stress in rice. Harbin： Northeast Forestry University， 2021.
	彭木. 生癌肠杆菌JY65的分离及其缓解水稻NaCl胁迫的分子机制解析. 哈尔滨：东北林业大学， 2021.
[36]	Nascimento F X， Rossi M J， Glick B R. Ethylene and 1-aminocyclopropane-1-carboxylate （ACC） in plant-bacterial interactions. Frontiers in Plant Science， 2018， 9： 114.
[37]	Ali S， Charles T C， Glick B R， et al. ACC deaminase activity in Pseudomonas spp. improves tomato growth under salinity. Plant and Soil， 2014， 374（1/2）： 45-56.
[38]	Zhu J K. Salt and drought stress signal transduction in plants. Annual Review of Plant Biology， 2002， 53： 247-273.
[39]	Chieb M， Gachomo E W. The role of plant growth promoting rhizobacteria in plant drought stress responses. BMC Plant Biology， 2023， 23（1）： 407.
[40]	Szabados L， Savouré A. Proline： A multifunctional amino acid. Trends in Plant Science， 2010， 15（2）： 89-97.
[41]	Liu Y F， Peng H， Wang W W， et al. Research progress on physiological and molecular mechanisms of plant salt tolerance. Jiangsu Agricultural Sciences， 2019， 47（12）： 30-36.
	刘云芬，彭华，王薇薇，等. 植物耐盐性生理与分子机制研究进展. 江苏农业科学， 2019， 47（12）： 30-36.
[42]	Gill S S， Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry， 2010， 48（12）： 909-930.
[43]	Foyer C H， Noctor G. Ascorbate and glutathione： The heart of the redox hub. Plant Physiology， 2011， 155（1）： 2-18.
[44]	Zhao J， Xie H J， Zhang J. Microbial diversity and physicochemical properties of rhizosphere microenvironment in saline-alkali soils of the yellow river delta. Environmental Science， 2020， 41（3）： 1449-1455.
	赵娇，谢慧君，张建. 黄河三角洲盐碱土根际微环境的微生物多样性及理化性质分析. 环境科学， 2020， 41（3）： 1449-1455.
[45]	Singh R P， Jha P N. The multifarious PGPR Serratia marcescens CDP-13 augments induced systemic resistance and enhanced salinity tolerance of wheat （Triticum aestivum L.）. PLoS One， 2016， 11（6）： e0155026.
[46]	Chen Y H， Lin H P， Xu S Q， et al. Screening of plant growth-promoting rhizobacterium with salt tolerance from rhizosphere. Acta Microbiologica Sinica， 2025， 65（1）： 150-168.
	陈燕鸿，蔺红苹，徐苏琪，等. 植物根际促生菌的筛选及其耐盐促生效果. 微生物学报， 2025， 65（1）： 150-168.
[47]	Qin J Z， Qin Z F， Ni G， et al. Advances in the separate functions or cross-kingdom interactions of AMF and PGPR in enhancing plant salt tolerance. Journal of Plant Nutrition and Fertilizers， 2024， 30（7）： 1354-1366.
	秦敬泽，秦泽峰，倪刚，等. AMF和PGPR单独或“跨界”互作促进植物耐盐性的研究进展. 植物营养与肥料学报， 2024， 30（7）： 1354-1366.
[48]	Sharma S， Kaur J， Bhardwaj R， et al. Enterobacter-mediated pH modulation enhances phosphorus availability in saline soils. Plant and Soil， 2020， 447： 89-103.
[49]	Li H， Qiu Y Z， Zhang X， et al. pH regulation in the rhizosphere by beneficial bacteria. Frontiers in Plant Science， 2022， 13： 893837.
[50]	Burns R G， De Forest J L， Marxsen J， et al. Soil enzymes in a changing environment： Current knowledge and future directions. Soil Biology and Biochemistry， 2013， 58： 216-234.
[51]	Dick R P. Soil enzyme activities as indicators of soil quality. SSSA Special Publication， 1994， 35： 107-124.
[52]	Nannipieri P， Trasar-Cepeda C， Dick R P. Soil enzyme activity： A brief history and biochemistry as a basis for appropriate interpretations. Soil Biology and Biochemistry， 2018， 118： 1-4.
[53]	Allison S D， Vitousek P M. Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biology and Biochemistry， 2005， 37（5）： 937-944.
[54]	Richardson A E， Hocking P J， Simpson R J， et al. Plant mechanisms to optimise access to soil phosphorus. Crop and Pasture Science， 2009， 60（2）： 124-143.
[55]	Ragot S A， Kertesz M A， Bünemann E K. phoD alkaline phosphatase gene diversity in soil. Applied and Environmental Microbiology， 2015， 81（20）： 7281-7289.
[56]	Sharma S B， Sayyed R Z， Trivedi M H， et al. Phosphate solubilizing microbes： sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus， 2013， 2： 587.
[57]	Ogawa N， Tzeng Y L， Zhou W， et al. Polyphosphate metabolism in environmental bacteria： Roles in stress survival and phosphorus cycling. Microbial Biotechnology， 2021， 14（3）： 756-769.
[58]	Yuan H M， Zhang X X， Chen X Y， et al. Salt stress reduces microbial phosphorus availability in coastal soils. Soil Biology and Biochemistry， 2020， 142： 107721.
[59]	Etesami H， Jeong B R， Glick B R. Contribution of arbuscular mycorrhizal fungi， phosphate-solubilizing bacteria， and silicon to P uptake by plant. Frontiers in Plant Science， 2021， 12： 699618.