Physiological Mechanisms Underlying the Modulation of Abiotic Stress Tolerance in Perennial Ryegrass by Bacillus paralicheniformis

doi:10.11733/j.issn.1007-0435.2026.07.009

Acta Agrestia Sinica ›› 2026, Vol. 34 ›› Issue (7): 2440-2449.DOI: 10.11733/j.issn.1007-0435.2026.07.009

Physiological Mechanisms Underlying the Modulation of Abiotic Stress Tolerance in Perennial Ryegrass by Bacillus paralicheniformis

YU Qiao¹, WANG He-tong¹, YANG Wan-qiang¹, MENG Qing-xian¹, ZHANG Yu-jing², PUBU Zhuoma³, HU Tian-ming¹, FU Juan-juan¹

1. College of Grassland Agriculture, Northwest A&F University, Yangling, Shaanxi Province 712100, China;
2. Bayannur Cultivated Land Quality Monitoring and Protection Center, Bayannur, Inner Mongolia 015000, China;
3. Institute of Grassland Science, Xizang Academy of Agricultural and Animal Husbandry Sciences, Lhasa, Xizang 850000, China

Received:2025-11-28 Revised:2026-01-28 Published:2026-07-02

副地衣芽孢杆菌对多年生黑麦草非生物胁迫抗性的生理调控机制

于乔¹, 王鹤潼¹, 杨万强¹, 孟庆娴¹, 张宇婧², 普布卓玛³, 呼天明¹, 付娟娟¹

1. 西北农林科技大学草业与草原学院, 陕西杨凌 712100;
2. 巴彦淖尔市耕地质量监测保护中心, 内蒙古巴彦淖尔 015000;
3. 西藏自治区农牧科学院草业科学研究所, 西藏拉萨 850000

通讯作者: 付娟娟，E-mail:fujuanjuan@nwafu.edu.cn
作者简介:于乔（2001-），男，汉族，吉林四平人，硕士研究生，主要从事植物与微生物互作研究，E-mail:2229300337@qq.com
基金资助:
西藏自治区重点研发及转化项目-二次科考项目（XZ202502ZY0050）资助

Abstract

Abstract: To investigate the physiological regulation mechanisms of plant growth-promoting bacteria on the drought， cold， and saline-alkali stress tolerance of perennial ryegrass （Lolium perenne L.）， this study used Bacillus paralicheniformis （NCBI ID： PRJNA1402526） as the test strain. A pot inoculation experiment was conducted under three abiotic stress conditions-drought， cold， and saline-alkali stress—to analyze the effects of rhizosphere inoculation on the growth indices， physiological characteristics， and root morphology of perennial ryegrass. The results showed that inoculation with B. paralicheniformis significantly alleviated the growth inhibition caused by abiotic stresses. Compared to the non-inoculated control， the inoculated plants exhibited significantly increased plant height， above-ground and below-ground biomass， along with markedly reduced leaf relative conductivity and malondialdehyde content. Additionally， the activities of superoxide dismutase， peroxidase， and catalase， as well as the contents of proline and soluble sugars， were significantly enhanced （P<0.05）. Moreover， root system architecture was notably improved. In conclusion， inoculation with B. paralicheniformis can significantly enhance the resistance of perennial ryegrass to drought， cold， and saline-alkali stresses by synergistically strengthening its antioxidant defense capacity， osmoregulatory function， and root morphological configuration.

Key words: Bacillus paralicheniformis, Perennial ryegrass, Abiotic stress, Antioxidant enzymes, Osmotic regulation, Root morphology

摘要： 为探究植物生长促生菌对多年生黑麦草（Lolium perenne L.）抗旱、抗寒及耐盐碱能力的生理调控机制，本研究以副地衣芽孢杆菌（Bacillus paralicheniformis， NCBI ID： PRJNA1402526）菌株为研究对象，采用盆栽接菌试验，设置干旱、低温、盐碱三种非生物胁迫处理，分析根际接种该菌株对多年生黑麦草生长指标、生理特性及根系形态的影响。发现接种副地衣芽孢杆菌显著缓解了非生物胁迫对多年生黑麦草生长的抑制。与未接种相比，接种处理的株高、地上部和地下部生物量均显著提高，叶片相对电导率和丙二醛含量显著降低，超氧化物歧化酶、过氧化物酶、过氧化氢酶活性及脯氨酸、可溶性糖含量显著上升，且根系形态构型得到显著改善（P<0.05）。综上，接种副地衣芽孢杆菌可通过协同增强多年生黑麦草的抗氧化防御能力、渗透调节功能及根系构型，从而显著提高其对干旱、低温和盐碱胁迫的抗性。

关键词: 副地衣芽孢杆菌, 多年生黑麦草, 非生物胁迫, 抗氧化酶, 渗透调节, 根系形态

CLC Number:

S543+.6

YU Qiao, WANG He-tong, YANG Wan-qiang, MENG Qing-xian, ZHANG Yu-jing, PUBU Zhuoma, HU Tian-ming, FU Juan-juan. Physiological Mechanisms Underlying the Modulation of Abiotic Stress Tolerance in Perennial Ryegrass by Bacillus paralicheniformis[J]. Acta Agrestia Sinica, 2026, 34(7): 2440-2449.

于乔, 王鹤潼, 杨万强, 孟庆娴, 张宇婧, 普布卓玛, 呼天明, 付娟娟. 副地衣芽孢杆菌对多年生黑麦草非生物胁迫抗性的生理调控机制[J]. 草地学报, 2026, 34(7): 2440-2449.

References

[1] PEI B, ZHANG G C, ZHANG S Y, et al. Effects of soil drought stress on photosynthetic characteristics and antioxidant enzyme activities in Hippophae rhamnoides Linn.seedings[J]. Acta Ecologica Sinica, 2013, 33(5):1386-1396 裴斌, 张光灿, 张淑勇, 等. 土壤干旱胁迫对沙棘叶片光合作用和抗氧化酶活性的影响[J]. 生态学报, 2013, 33(5):1386-1396
[2] JIANG F Y, LI Y, WENG B Q. Review on physiology of chilling stress and chilling resistance of plants[J]. Fujian Journal of Agricultural Sciences, 2002, 17(3):190-195 江福英, 李延, 翁伯琦. 植物低温胁迫及其抗性生理[J]. 福建农业学报, 2002, 17(3):190-195
[3] WANG Q Z, LIU Q, GAO Y N, et al. Review on the mechanisms of the response to salinity-alkalinity stress in plants[J]. Acta Ecologica Sinica, 2017, 37(16):5565-5577 王佺珍, 刘倩, 高娅妮, 等. 植物对盐碱胁迫的响应机制研究进展[J]. 生态学报, 2017, 37(16):5565-5577
[4] LUGTENBERG B, KAMILOVA F. Plant-growth-promoting rhizobacteria[J]. Annual Review of Microbiology, 2009, 63:541-556
[5] SHRIVASTAVA P, KUMAR R. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation[J]. Saudi Journal of Biological Sciences, 2015, 22(2):123-131
[6] EGAMBERDIEVA D, DAVRANOV K, WIRTH S, et al. Impact of soil salinity on the plant-growth-promoting and biological control abilities of root associated bacteria[J]. Saudi Journal of Biological Sciences, 2017, 24(7):1601-1608
[7] SHAFI J, TIAN H, JI M S. Bacillus species as versatile weapons for plant pathogens: a review[J]. Biotechnology & Biotechnological Equipment, 2017, 31(3):446-459
[8] VESSEY J K. Plant growth promoting rhizobacteria as biofertilizers[J]. Plant and Soil, 2003, 255(2):571-586
[9] LIU S W, JIANG Y W. Identification of differentially expressed genes under drought stress in perennial ryegrass[J]. Physiologia Plantarum, 2010, 139(4):375-387
[10] LEI J Q, ZHANG Q, ZHU Z H, et al. Molecular modification and host optimization enhance the expression ofγ-glutamyltranspeptidase in Bacillus licheniformis[J]. Chinese Journal of Biotechnology, 2025, 41(5):2026-2037 雷家琪, 张清, 祝志豪, 等. 基于分子改造和宿主优化促地衣芽胞杆菌高效表达γ-谷氨酰转肽酶[J]. 生物工程学报, 2025, 41(5):2026-2037
[11] LIU P, CUI T T, SUN P Y, et al. Effects of Arthrobacter psychrolactophilus B7 on the growth and antioxidant defense system in perennial ryegrass under shade stress[J]. Pratacultural Science, 2021, 38(1):81-88 刘鹏, 崔彤彤, 孙鹏越, 等. 嗜冷乳糖节杆菌B7对遮阴胁迫下多年生黑麦草幼苗生长和抗氧化防御系统的影响[J]. 草业科学, 2021, 38(1):81-88
[12] WANG Y X. Colonization of the biocontrol strain Bacillus paralicheniformis ZYGT1811 in wheat plants and rhizosphere and its genomic analysis[D]. Lanzhou:Gansu Agricultural University, 2025:15-28 王艺璇. 生防副地衣芽孢杆菌ZYGT1811在小麦植株和根际的定殖及其基因组学分析[D]. 兰州:甘肃农业大学, 2025:15-28
[13] TAN W R, ZHANG D W, ZHOU H P, et al. Transcription factor HAT1 is a substrate of SnRK_2.3 kinase and negatively regulates ABA synthesis and signaling in Arabidopsis responding to drought[J]. Plos Genetics, 2018, 14(4):e1007336
[14] ZHU Z, JIANG J Y, JIANG C J, et al. Effects of low temperature stress on SOD activity, soluble protein content and soluble sugar content in Camellia sinensis leaves[J]. Journal of Anhui Agricultural University, 2011, 38(1):24-26 朱政, 蒋家月, 江昌俊, 等. 低温胁迫对茶树叶片SOD、可溶性蛋白和可溶性糖含量的影响[J]. 安徽农业大学学报, 2011, 38(1):24-26
[15] LI S X, LIU J L, AN Y R, et al. MsPIP2；2, a novel aquaporin gene from Medicago sativa, confers salt tolerance in transgenic Arabidopsis[J]. Environmental and Experimental Botany, 2019, 165:39-52
[16] LI H S. Principles and Techniques of Plant Physiological and Biochemical Experiments [M]. Beijing: Higher Education Press, 2000: 279-298 李合生. 植物生理生化实验原理和技术[M]. 北京:高等教育出版社, 2000:279-298
[17] TANG L S. Morphological, physiological and molecular response mechanism of Cynodon dactylon in Xinjiang under alkaline salt stress[D]. Urumqi:Xinjiang Agricultural University, 2024:20-30 汤丽斯. 碱性盐胁迫下新疆狗牙根形态、生理及分子响应机制研究[D]. 乌鲁木齐:新疆农业大学, 2024:20-30
[18] HAMMERSCHMIDT R, NUCKLES E M, KUĆ J. Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium[J]. Physiological Plant Pathology, 1982, 20(1):73-82
[19] CAKMAK I, MARSCHNER H. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves[J]. Plant Physiology, 1992, 98(4):1222-1227
[20] YANG Q. Effects of exogenous melatonin on seed germination and seedling growth of ornamental buckwheat under high temperature stress[D]. Baoding:Hebei Agricultural University, 2023:15-20 杨芊. 外源褪黑素对高温胁迫下观赏荞麦种子萌发及幼苗生长的影响[D]. 保定:河北农业大学, 2023:15-20
[21] HUANG Z Y, WANG Y Y, MA S T, et al. Interactive effects of cultivar and planting density on root morphology of summer maize[J]. Chinese Journal of Ecology, 2025, 44(11):3613-3619 黄紫岳, 王园园, 马守田, 等. 种植品种与密度互作对玉米根系形态的影响[J]. 生态学杂志, 2025, 44(11):3613-3619
[22] LIN F C, LI D B. Cell-lyric effect of Bacillus subtilis on plant fungal pathogens[J]. Acta Phytopathologica Sinica, 2003, 33(2):174-177 林福呈, 李德葆. 枯草芽孢杆菌(Bacilllus subtilis)S₉对植物病原真菌的溶菌作用[J]. 植物病理学报, 2003, 33(2):174-177
[23] ZHANG Q. Research progress on response of wheat to soil water stress[J]. Modern Agricultural Science and Technology, 2024(18):31-34 张琴. 小麦对土壤水分胁迫响应的研究进展[J]. 现代农业科技, 2024(18):31-34
[24] HU J C, XUE D L, MA C X, et al. Research advances in plant growth-promoting rhizobacteria and its application prospects[J]. Chinese Journal of Applied Ecology, 2004, 15(10):1963-1966 胡江春, 薛德林, 马成新, 等. 植物根际促生菌(PGPR)的研究与应用前景[J]. 应用生态学报, 2004, 15(10):1963-1966
[25] ESITKEN A, YILDIZ H E, ERCISLI S, et al. Effects of plant growth promoting bacteria (PGPB) on yield, growth and nutrient contents of organically grown strawberry[J]. Scientia Horticulturae, 2010, 124(1):62-66
[26] GUO Q Q, ZHOU W B. Advances in the mechanism underlying plant response to stress combination[J]. Chinese Bulletin of Botany, 2019, 54(5):662-672 郭倩倩, 周文彬. 植物响应联合胁迫机制的研究进展[J]. 植物学报, 2019, 54(5):662-672
[27] ABDELAZIZ M E, ABDELSATTAR M, ABDELDAYM E A, et al. Piriformospora indica alters Na+/K+ homeostasis, antioxidant enzymes and LeNHX1 expression of greenhouse tomato grown under salt stress[J]. Scientia Horticulturae, 2019, 256:108532
[28] HAN Q Q, LÜ X P, BAI J P, et al. Beneficial soil bacterium Bacillus subtilis (GB03) augments salt tolerance of white clover[J]. Frontiers in Plant Science, 2014, 5:525
[29] ASHRAFI E, RAZMJOO J, ZAHEDI M, et al. Screening alfalfa for salt tolerance based on lipid peroxidation and antioxidant enzymes[J]. Agronomy Journal, 2015, 107(1):167-173
[30] MA X J, OUYANG Z P, LUO HB, et al. Bacillus velezensis HR6-1 enhances salt tolerance in tomato by increasing endogenous cytokinin content and improving ROS scavenging[J]. Microbiological Research, 2025, 296:128143

Physiological Mechanisms Underlying the Modulation of Abiotic Stress Tolerance in Perennial Ryegrass by Bacillus paralicheniformis

副地衣芽孢杆菌对多年生黑麦草非生物胁迫抗性的生理调控机制

PDF

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	DU Xin-wei, RONG Rui-wei, HUA Yi-wen, LIU Yi, TAO Jia-li, ZHOU Si-yi, XU Tao, CEN Hui-fang, ZHU Hui-sen. Cloning MsLAC17 Gene and Analysis of its Response to Abiotic Stress in Medicago sativa ‘Pianguan’ [J]. Acta Agrestia Sinica, 2026, 34(6): 2022-2031.
[2]	LIU Jin-di, CHEN Shi-yong, LI Jin, LIANG Guo-ling, ZHOU Qing-ping. The Identification of the SWEET Gene Family in Oats and Its Expression Analysis in Response to Drought and Salt Stress [J]. Acta Agrestia Sinica, 2026, 34(5): 1568-1583.
[3]	XU Yi, WANG Ting, GUO Yu-peng, MIAO Xing-fen, ZHENG Xia, SHI Peng-jun. Evaluation and Screening of Reference Genes in Alfalfa （Medicago sativa L. ‘Gongnong No.1’） Different Tissues under Waterlogging Stress [J]. Acta Agrestia Sinica, 2026, 34(4): 1146-1157.
[4]	FENG Zi-xuan, XU Zi-ying, MA Hong-yan, JING Jing-ying. Effects of Phosphorus Addition on Biomass and Root Plasticity of Different Alfalfa Varieties [J]. Acta Agrestia Sinica, 2026, 34(2): 392-402.
[5]	LI Di-na, WANG Kai, TAO Jia-li, XU Tao, LI Qing-xiu, ZHU Hui-sen, CEN Hui-fang. Cloning， Subcellular Localization and Expression Analysis of MsMYB44 Gene of Medicago sativa‘Pianguan’ [J]. Acta Agrestia Sinica, 2026, 34(1): 33-42.
[6]	CHEN Cai-jin, MA Lin, BAO Ming-fang, JIANG Qing-xue, ZHANG Guo-hui, ZHANG Shang-pei, GAO Ting, LIU Wen-hui, WANG Xue-min. Research Progress on the Role of WRKY Family Genes in Plants [J]. Acta Agrestia Sinica, 2025, 33(7): 2059-2069.
[7]	YAN San-bo, CAI Jia-bang, WANG Yang, ZHANG Xin-quan, NIE Gang. Effects of Exogenous Salicylic Acid on Seed Germination of Perennial Ryegrass under High Temperature Stress [J]. Acta Agrestia Sinica, 2025, 33(3): 968-974.
[8]	LUO Li-xuan, ZHOU Tao, XU Qian, LU Rui, LIU Ning-fang, HU Long-xing. Bioinformatics Analysis of GATA Family of Pennisetum glaucum [J]. Acta Agrestia Sinica, 2025, 33(2): 391-400.
[9]	WANG Ning-bin, QIAO Ji-rong, LI Shao-yu, ZHENG Jia-hua, ZHANG Feng, ZHANG Bin, XU Long-chao, ZHOU Qing-ge, CHEN Xin-li, ZHAO Meng-li, JI Xiang. Effects of Grazing Intensity on Root Morphology of Stipa breviflora [J]. Acta Agrestia Sinica, 2025, 33(12): 4015-4022.
[10]	GAO Shou-yu, XIANG Qing-yuan, MA Jing-ru, LI Yu-ying, XIA Fang-shan. Selection and Validation of Reference Genes for qRT-PCR in Bothriochloa ischaemum seedlings under Abiotic Stresses [J]. Acta Agrestia Sinica, 2025, 33(11): 3559-3570.
[11]	ZHOU Yi-fan, YANG Zhao, SUI Xiao-qing, LANG Meng-qing, Jirge, LIU Hai-jun, YE Yi-zhen. Effect of 2，4-Epibrassinolide on the Physiological Properties of Bromus inermis Under Salt Stress [J]. Acta Agrestia Sinica, 2025, 33(11): 3732-3740.
[12]	LU Shuang, LIU Yue-yue, MAO Jia-jing, XU Xin-yu, LUO Li-wei, HAN Lie-bao, XU Li-xin. Preliminary Analysis on Cold Resistance of Zoysia japonica Mutant Plant Zjsgr in Beijing District [J]. Acta Agrestia Sinica, 2025, 33(1): 28-33.
[13]	LIANG Qing-wei, YANG Xiu-fang, NA Ri-su, YU Xue-ran, HAN Xiao-hua. Effects of Last Cutting on Root Neck Antioxidation of Three Fall Dormancy Rating Alfalfa Varieties [J]. Acta Agrestia Sinica, 2025, 33(1): 119-124.
[14]	ZOU Wei-peng, ZHAI Jia-xing, LI Di-na, HUANG Jie-qiong, GUO Kang-jie, CEN Hui-fang, ZHU Hui-sen, XU Tao. Identification of Alfalfa NAC Gene Family and Analysis of Their Expression Patterns under Abiotic Stress [J]. Acta Agrestia Sinica, 2024, 32(8): 2440-2458.
[15]	LIU Xue-ting, SHI Feng-ling, YE Wen-xing. Analysis of Antioxidant Characteristics of Exogenous Inositol on Poa pratensis L. in Response to Drought Stress [J]. Acta Agrestia Sinica, 2024, 32(8): 2584-2591.