Physiological Responses and Molecular Regulatory Characteristics of Suaeda salsa under Fluoroquinolone Antibiotic Stress

doi:10.7525/j.issn.1673-5102.2026.04.012

Abstract

Abstract:

Fluoroquinolone antibiotics（FQs） are widely detected in agricultural irrigation water， livestock wastewater， and coastal wetlands， posing potential stress to plant growth and ecological processes. Taking ofloxacin（OFX） and enrofloxacin（ENR） as representative compounds， this study employed physiological and biochemical assays in combination with transcriptomic analysis to systematically elucidate the physiological responses and molecular regulatory mechanisms of Suaeda salsa under FQs stress. The results showed that both OFX and ENR induced significant oxidative stress in both the aboveground and belowground parts of S. salsa. Comparatively， ENR caused more pronounced lipid peroxidation， which was accompanied by the significant differential expression of genes related to phenylpropanoid metabolism and ABC（ATP-binding cassette） transporters. In contrast， OFX stress primarily impaired photosystem structure and function， while simultaneously enhancing antioxidant defense through the regulation of the WRKY transcription factor family and MAPK（mitogen-activated protein kinase） signaling pathways. Furthermore， both antibiotic treatments promoted the glycolysis-pyruvate metabolism pathway， thereby providing sustained energy supply and reducing power to support stress resistance. Collectively， under FQs stress， S. salsa exhibited a multi-level adaptive response strategy driven by the coordinated regulation of structural defense， metabolic reprogramming， and signaling pathways.

Key words: Suaeda salsa, fluoroquinolone antibiotics, phenylpropanoid metabolism, antioxidant system, phytoremediation

CLC Number:

Q948.1

Peize GUAN, Peijing KUANG, Yuting WEI, Zihan GUAN, Ke ZHAO, Yubo CUI. Physiological Responses and Molecular Regulatory Characteristics of Suaeda salsa under Fluoroquinolone Antibiotic Stress[J]. Bulletin of Botanical Research, 2026, 46(4): 712-727.

Figures/Tables 12

Table 1

Table 2

Fig.1

Fig.2

Fig.3

Fig.4

Fig.5

Table 3

Fig.6

Fig.7

Fig.8

Fig.9

References 48

[1]	付雨，剧泽佳，付耀萱，等.白洋淀优势水生植物中喹诺酮类抗生素的生物富集特征及其与环境因子相关性研究［J］.环境科学学报，2021，41（9）：3620-3630.
	Fu Yu， Ju Zejia， Fu Yaoxuan，et al.The bioaccumulation of quinolones（QNs） in the dominant macrophytes and the correlation with environmental factors in Baiyangdian Lake［J］.Acta Scientiae Circumstantiae，2021，41（9）：3620-3630.
[2]	吴涵，赵健，张华民，等.黄河下游典型水体中医药类新污染物分布特征及生态风险评价［J］.环境科学学报，2024，44（9）：293-301.
	Wu Han， Zhao Jian， Zhang Huamin，et al.Distribution characteristics and ecological risk assessment of emerging pharmaceutical contaminants in typical water bodies of the Lower Yellow River［J］.Acta Scientiae Circumstantiae，2024，44（9）：293-301.
[3]	Wen L L， Dai J J， Ma J，et al.Comprehensive profiling of quinolone antibiotics in the Bohai Sea：occurrence，source apportionment，and environmental risks［J］.Environmental Pollution，2025，387：127338.
[4]	Wen L L， Dai J J， Song J M，et al.Dual-source fingerprints and ecological risks of quinolone antibiotics in the Yellow Sea：implications for resistance and management［J］.Environmental Chemistry and Ecotoxicology，2026，8：89-100.
[5]	陈昳鸥，李玥，沈嘉怡，等.土霉素对油菜次生代谢及抗氧化作用的影响［J］.生态毒理学报，2025，20（1）：148-155.
	Chen Yi’ou， Li Yue， Shen Jiayi，et al.Effects of oxytetracycline on secondary metabolism and antioxidant activity of rapeseed［J］.Asian Journal of Ecotoxicology，2025，20（1）：148-155.
[6]	Chen L L， Xu Z L， He Y Q，et al.Multiomics analysis reveals key targeted metabolic pathways underlying the hormesis and detrimental effects of enrofloxacin on rice plants［J］.Journal of Agricultural and Food Chemistry，2025，73（4）：2678-2695.
[7]	Zhang Z H， Liu X N， Li N，et al.Effect of ofloxacin levels on growth，photosynthesis and chlorophyll fluorescence kinetics in tomato［J］.Plant Physiology and Biochemistry，2023，194：374-382.
[8]	Jin J J， Xu L L， Zhang S Y，et al.Oxidative response of rice（Oryza sativa L.） seedlings to quinolone antibiotics and its correlation with phyllosphere microbes and antibiotic resistance genes［J］.Science of the Total Environment，2023，867：161544.
[9]	Mu X Y， Zhang S H， Lu J H，et al.Fate and removal of fluoroquinolone antibiotics in mesocosmic wetlands：impact on wetland performance，resistance genes and microbial communities［J］.Journal of Hazardous Materials，2024，470：133740.
[10]	温丽联，宋金明，李学刚，等.氟喹诺酮类抗生素的环境污染及其对微生物介导氮循环的影响［J］.应用生态学报，2023，34（11）：3114-3126.
	Wen Lilian， Song Jinming， Li Xuegang，et al.Environmental pollution of fluoroquinolones and its relationship with nitrogen cycling mediated by microorganisms［J］.Chinese Journal of Applied Ecology，2023，34（11）：3114-3126.
[11]	Barroso G M， dos Santos E A， Pires F R，et al.Phytoremediation：a green and low-cost technology to remediate herbicides in the environment［J］.Chemosphere，2023，334：138943.
[12]	荣渝虹，张发明，杨娟，等.香根草对磺胺类抗生素污染水体的修复潜力研究［J］.生态与农村环境学报，2022，38（6）：795-801.
	Rong Yuhong， Zhang Faming， Yang Juan，et al.Studies on phytoremediation potentials of Vetiveria zizanioides to sulfonamides polluted water［J］.Journal of Ecology and Rural Environment，2022，38（6）：795-801.
[13]	Panja S， Sarkar D， Zhang Z M，et al.Removal of antibiotics and nutrients by vetiver grass（Chrysopogon zizanioides） from a plug flow reactor based constructed wetland model［J］.Toxics，2021，9（4）：84.
[14]	Huang W J， Kong R， Chen L J，et al.Physiological responses and antibiotic-degradation capacity of duckweed （Lemna aequinoctialis） exposed to streptomycin［J］.Frontiers in Plant Science，2022，13：1065199.
[15]	Zhou T， An Q Y， Zhang L，et al.Phytoremediation for antibiotics removal from aqueous solutions：a meta-analysis［J］.Environmental Research，2024，240：117516.
[16]	Li Q， Song J.Analysis of widely targeted metabolites of the euhalophyte Suaeda salsa under saline conditions provides new insights into salt tolerance and nutritional value in halophytic species［J］.BMC Plant Biology，2019，19（1）：388.
[17]	Shang C L， Wang L， Tian C Y，et al.Heavy metal tolerance and potential for remediation of heavy metal-contaminated saline soils for the euhalophyte Suaeda salsa ［J］.Plant Signaling & Behavior，2020，15（11）：1805902.
[18]	Dong X， Liu Y， Ma X F，et al.Disclosing the effect of exogenous betaine on growth of Suaeda salsa（L.） Pall in the Liaohe coastal wetland，North China［J］.Marine Pollution Bulletin，2024，198：115852.
[19]	Badawy S， Yang Y Q， Liu Y N，et al.Toxicity induced by ciprofloxacin and enrofloxacin：oxidative stress and metabolism［J］.Critical Reviews in Toxicology，2021，51（9）：754-787.
[20]	Wang H， Jin M K， Xu L L，et al.Effects of ketoprofen on rice seedlings：insights from photosynthesis，antioxidative stress，gene expression patterns，and integrated biomarker response analysis［J］.Environmental Pollution，2020，263：114533.
[21]	Mihailova G， Kocheva K， Goltsev V，et al.Application of a diffusion model to measure ion leakage of resurrection plant leaves undergoing desiccation［J］.Plant Physiology and Biochemistry，2018，125：185-192.
[22]	Farooq M A， Islam F， Ayyaz A，et al.Mitigation effects of exogenous melatonin-selenium nanoparticles on arsenic-induced stress in Brassica napus ［J］.Environmental Pollution，2022，292：118473.
[23]	Zhang P， Shen L Q， Chen J Y，et al.Comparative study of the toxicity mechanisms of quinolone antibiotics on soybean seedlings：insights from molecular docking and transcriptomic analysis［J］.Science of the Total Environment，2023，896：165254.
[24]	Du J， Liu Q H， Pan Y，et al.The research status，potential hazards and toxicological mechanisms of fluoroquinolone antibiotics in the environment［J］.Antibiotics，2023，12（6）：1058.
[25]	Xiao W Y， Bian Z Y.Impact of molecular structure on the biological removal efficiency of fluoroquinolone antibiotics：an in-silico approach［J］.Science of the Total Environment，2024，956：177178.
[26]	Zhang H H， Zeng N D， Feng Q R，et al.New mechanistic insights into PAHs transport across wheat root cell membrane：evidence for ABC transporter mediation［J］.Science of the Total Environment，2023，859：160251.
[27]	Nybom I， Bucheli T D， Garland G.Antibiotics uptake from soil and translocation in the plants-meta-analysis［J］.Chimia，2024，78（4）：209-214.
[28]	Jin M K， Yang Y T， Zhao C X，et al.ROS as a key player in quinolone antibiotic stress on Arabidopsis thaliana：from the perspective of photosystem function，oxidative stress and phyllosphere microbiome［J］.Science of the Total Environment，2022，848：157821.
[29]	Singh V， Pandey B， Suthar S.Phytotoxicity and degradation of antibiotic ofloxacin in duckweed（Spirodela polyrhiza） system［J］.Ecotoxicology and Environmental Safety，2019，179：88-95.
[30]	Carballo M， Rodríguez A， de la Torre A.Phytotoxic effects of antibiotics on terrestrial crop plants and wild plants：a systematic review［J］.Archives of Environmental Contamination and Toxicology，2022，82（1）：48-61.
[31]	Chen X H， Song Y X， Ling C，et al.Fate of emerging antibiotics in soil-plant systems：a case on fluoroquinolones［J］.Science of the Total Environment，2024，951：175487.
[32]	Wang M L， Wang Y D， Li X Z，et al.Integration of metabolomics and transcriptomics reveals the regulation mechanism of the phenylpropanoid biosynthesis pathway in insect resistance traits in Solanum habrochaites ［J］.Horticulture Research，2024，11（2）：uhad277.
[33]	Liu X N， Lv Y， Gao S，et al.Ofloxacin induces etiolation in welsh onion leaves［J］.Chemosphere，2021，267：128918.
[34]	Vicidomini C， Palumbo R， Moccia M，et al.Oxidative processes and xenobiotic metabolism in plants：mechanisms of defense and potential therapeutic implications［J］.Journal of Xenobiotics，2024，14（4）：1541-1569.
[35]	Xu Y， Fu X Y.Reprogramming of plant central metabolism in response to abiotic stresses：a metabolomics view［J］.International Journal of Molecular Sciences，2022，23（10）：5716.
[36]	Wang B， Xu H， Liu Y，et al.Unraveling phytoremediation mechanisms of the common reed（Phragmites australis） suspension cells towards ciprofloxacin：xenobiotic transformation and metabolic reprogramming［J］.Water Research，2024，266：122347.
[37]	Javed T， Gao S J.WRKY transcription factors in plant defense［J］.Trends in Genetics，2023，39（10）：787-801.
[38]	Yoon J， Choi H， An G.Roles of lignin biosynthesis and regulatory genes in plant development［J］.Journal of Integrative Plant Biology，2015，57（11）：902-912.
[39]	Aristilde L， Melis A， Sposito G.Inhibition of photosynthesis by a fluoroquinolone antibiotic［J］.Environmental Science & Technology，2010，44（4）：1444-1450.
[40]	Riaz L， Mahmood T， Coyne M S，et al.Physiological and antioxidant response of wheat（Triticum aestivum） seedlings to fluoroquinolone antibiotics［J］.Chemosphere，2017，177：250-257.
[41]	Wu X J， Chen X D， Zhang D Z，et al.Integrative multi-omics analysis reveals the underlying toxicological mechanisms of enrofloxacin on the growth of wheat seedling roots［J］.Journal of Hazardous Materials，2024，477：135303.
[42]	Savchenko T， Tikhonov K.Oxidative stress-induced alteration of plant central metabolism［J］.Life，2021，11（4）： 304.
[43]	Bao L F， Wang W Y， Li M Y，et al.Reactive oxygen species-post translational modifications-central carbon metabolism regulatory loop：coordination of redox homeostasis and carbon flux allocation in plants under abiotic stress［J］.Frontiers in Plant Science，2025，16：1637328.
[44]	Liu Y K， He C Z.A review of redox signaling and the control of MAP kinase pathway in plants［J］.Redox Biology，2017，11：192-204.
[45]	Ninkuu V， Aluko O O， Yan J P，et al.Phenylpropanoids metabolism：recent insight into stress tolerance and plant development cues［J］.Frontiers in Plant Science，2025，16：1571825.
[46]	Bose Mazumdar A， Chattopadhyay S.Glutathione pathways and gene networks：central players in crop adaptation to environmental stresses［J］.Plant Growth Regulation，2025，105（6）：1927-1948.
[47]	Li Z H， Chen J， Xu L L，et al.Quinolone antibiotics inhibit the rice photosynthesis by targeting photosystem II center protein：generational differences and mechanistic insights［J］.Environmental Science & Technology，2024，58（26）：11280-11291.
[48]	Remy E， Duque P.Beyond cellular detoxification：a plethora of physiological roles for MDR transporter homologs in plants［J］.Frontiers in Physiology，2014，5：201.

时间 Time/min	流动相A百分比 Percentage of mobile phase A/%	流动相B百分比 Percentage of mobile phase B/%
（0~1.0］	98	2
（1.0~2.0］	98→2	2→98
（2.0~3.5］	2	98
（3.5~4.0］	2→98	98→2
（4.0~6.0］	98	2

分类 Category	基因 Gene	连接通路 Linked pathway	功能/作用方向 Function/direction of effect
ENR	PAL	Phenylpropanoid biosynthesis	木质素合成/防御反应
ENR	4CL	Phenylpropanoid biosynthesis	细胞壁增强
ENR	CYP450	Sulfur metabolism / Secondary metabolism	解毒与代谢调节
ENR	ABC transporter	Transport / Detoxification	外排抗生素
ENR	CAD	Phenylpropanoid biosynthesis	细胞壁加固/木质素合成
OFX	LHCA1	Photosystem I	光捕获、光系统功能
OFX	LHCB2	Photosystem Ⅱ antenna proteins	光能传递
OFX	PsbO	Photosystem Ⅱ	光系统稳定
OFX	WRKY TF	MAPK signaling / Plant-pathogen interaction	信号转导
OFX	MAPK	MAPK signaling pathway	逆境响应信号
COMMON	SOD	Glutathione metabolism / ROS scavenging	清除ROS
COMMON	CAT	Peroxisome / ROS scavenging	分解H₂O₂
COMMON	GST	Glutathione metabolism	抗氧化与解毒
COMMON	HSP	Protein processing in ER	抗逆保护
COMMON	ALDH	Pyruvate metabolism	碳流分配与能量供给