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刘磊
吉林 | 吉林农业大学 | 副教授
  邮箱   lei_liu_2020@163.com 
TA的实验室:   吉农刘磊lab
论文

Cadmium contamination impairs alkaline tolerance in sugar beet by inhibiting carbon fixation and tryptophan metabolism

期刊: Plant Physiology and Biochemistry  2025
作者: Zhijia Gai,Shuo Ye,Xinrui Zhou,Fawei Tang,Ruixin Qu,Zhiwei Wang,Xu Hu,Yang Liu,Donglin Li,Kepan Yang,Pengfei Zhang,Xiangnan Li,Lei Liu
DOI:10.1016/j.plaphy.2025.109857

Alkaline stress suppresses soybean waterlogging tolerance by exacerbating energy expenditure and ROS accumulation

期刊: Plant Physiology and Biochemistry  2025
作者: Ziyang Wang,Zhilong Li,Zhiwei Wang,Tianhao Liu,Peng Zhang,Shuxin Li,Shuo Ye,Kepan Yang,Zhijia Gai,Lei Liu
DOI:10.1016/j.plaphy.2025.110381

Proline–Nitrogen Metabolic Coordination Mediates Cold Priming-Induced Freezing Tolerance in Maize

Cold stress critically restricts maize seedling growth in Northeast China, yet the mechanism by which cold priming (CP) enhances cold tolerance through proline–nitrogen metabolic networks remains unclear. This study systematically investigated CP’s synergistic regulation in cold-tolerant (Heyu27) and cold-sensitive (Dunyu213) maize using a two-phase temperature regime (priming induction/stress response) with physiological and multivariate analyses. CP alleviated cold-induced photosynthetic inhibition while maintaining a higher chlorophyll and photosynthetic rate, though biomass responses showed varietal specificity, with Heyu27 minimizing growth loss through optimized carbon–nitrogen allocation. Antioxidant enzymes such as superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) were pre-activated during early stress, effectively scavenging reactive oxygen species (ROS) and reducing malondialdehyde (MDA) accumulation, with Heyu27 showing superior redox homeostasis. CP enhanced proline accumulation via bidirectional enzyme regulation (upregulating ∆1-pyrroline-5-carboxylate synthase/reductase [P5CS/P5CR], inhibiting proline dehydrogenase [ProDH]) and reprogrammed nitrogen metabolism through glutamate dehydrogenase/isocitrate dehydrogenase (GDH/ICDH)-mediated ammonium conversion to glutamate, alleviating nitrogen dysregulation while supplying proline precursors. Principal component analysis revealed divergent strategies: Heyu27 prioritized proline–antioxidant synergy, whereas Dunyu213 emphasized photosynthetic adjustments. These findings demonstrate that CP establishes “metabolic memory” through optimized proline–nitrogen coordination, synergistically enhancing osmoregulation, reactive oxygen species (ROS) scavenging, and nitrogen utilization. This study elucidates C4-specific cold adaptation mechanisms, advancing cold-resistant breeding and stress-resilient agronomy.

期刊: Plants  2025
作者: Zhijia Gai,Lei Liu,Na Zhang,Jingqi Liu,Lijun Cai,Xü Yang,Ao Zhang,Pengfei Zhang,Junjie Ding,Yifei Zhang
DOI:10.3390/plants14101415

Jasmonic Acid Signaling Pathway Mediates Decabromodiphenyl Ethane (DBDPE) Tolerance by Modulating Photosynthesis and Oxidative Stress in Sugar Beet: Insights from Integrative Physiological and Multiomics Analyses

期刊: Journal of Agricultural and Food Chemistry  2025
作者: Pengfei Zhang,Xuerui Wang,Lei Liu,Yao Meng,Zhijia Gai,Cong Wang,Yubo Wang,Shengwei Zhang,Wanrong Gu
DOI:10.1021/acs.jafc.4c11778

Soil microbes mediate the priming effect in response to 12 years of nitrogen management in different crop cultivation patterns

期刊: Applied Soil Ecology  2025
作者: Kepan Yang,Yali Liu,Shiqiang Ge,Chaoqun Zou,Lei Liu,Xiting Zhang
DOI:10.1016/j.apsoil.2024.105844

Salt priming induces low-temperature tolerance in sugar beet via xanthine metabolism

期刊: Plant Physiology and Biochemistry  2023
作者: Lei Liu,Pengfei Zhang,Guozhong Feng,Wenfeng Hou,Tianhao Liu,Zhijia Gai,Yanhui Shen,Xin Qiu,Xiangnan Li
DOI:10.1016/j.plaphy.2023.107810

Microbial Mechanisms of the Priming Effect over 12 Years of Different Amounts of Nitrogen Management

The return of crop residues and application of chemical nitrogen (N) can influence the soil organic carbon (SOC) turnover. However, the changes in the response of the priming effect (PE) to N management in real farming systems are not fully understood. In this research, we launched a 270-day in situ experiment in three N management plots (N0, no N; N1, 300 kg hm−2; and N2, 360 kg hm−2) on a long-term maize farm in order to examine the microbial mechanisms that trigger the PE in the presence of 13C-labeled maize residues. We found that N1 decreased SOC mineralization and the positive PE, but increased the residual C mineralization and microbial C use efficiency in comparison with N0 and N2, respectively. The positive PE can be explained by the microbial nutrient mining theory for N0 and by the microbial stoichiometry decomposition theory for N1 and N2, as reflected by the increased abundance of oligotrophic phyla in N0 and the increased abundance of copiotrophic phyla in N1 and N2. The microbial biomass C (MBC), residue-derived MBC, and the communities’ complexity were decreased in N2 due to the acidification of the soil environment, but N1 enhanced the MBC, residue-derived MBC, and bacterial communities’ complexity. The keystone bacterial taxa of Vicinamibacteraceae and Gemmatimonas preferred the recalcitrant C of SOC in N0 and N2, respectively. However, Acidibacter favored the labile residual C in N1. The keystone fungal taxa of Penicillium, Sarocladium, and Cladophialophora exhibited wide substrate-use abilities in N0, N1, and N2, respectively. Our research depicts the mechanisms of how microbial communities’ structures are reshaped through N management and emphasizes the functions of the keystone microbial taxa in C turnover and the PE in farming systems.

期刊: Agronomy  2023
作者: Kepan Yang,Peng Peng,Fuyuan Duan,Hu Tang,Kaixuan Wu,Zhenying Wu,Fan Li,Yong Chen,Chaoqun Zou,Lei Liu,Jianwu Wang
DOI:10.3390/agronomy13071783

Modulations in protein phosphorylation explain the physiological responses of barley (Hordeum vulgare) to nanoplastics and ZnO nanoparticles

期刊: Journal of Hazardous Materials  2023
作者: Junhong Guo,Shuxin Li,Marian Brestic,Na Li,Peng Zhang,Lei Liu,Xiangnan Li
DOI:10.1016/j.jhazmat.2022.130196

Salt stress improves the low-temperature tolerance in sugar beet in which carbohydrate metabolism and signal transduction are involved

期刊: Environmental and Experimental Botany  2023
作者: Lei Liu,Zhijia Gai,Xin Qiu,Tianhao Liu,Shuxin Li,Fan Ye,Shulian Jian,Yanhui Shen,Xiangnan Li
DOI:10.1016/j.envexpbot.2023.105239

2-Oxoglutarate contributes to the effect of foliar nitrogen on enhancing drought tolerance during flowering and grain yield of soybean

AbstractDrought severely affects the growth and yield of soybean plants especially during the flowering period. To investigate the effect of 2-oxoglutarate (2OG) in combination with foliar nitrogen (N) at flowering stage on drought resistance and seed yield of soybean under drought stress. This experiment was conducted in 2021 and 2022 on drought-resistant variety (Hefeng 50) and drought-sensitive variety (Hefeng 43) soybean plants treated with foliar N (DS + N) and 2-oxoglutarate (DS + 2OG) at flowering stage under drought stress. The results showed that drought stress at flowering stage significantly increased leaf malonaldehyde (MDA) content and reduced soybean yield per plant. However, superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT) activities were significantly increased by foliar N treatment, and 2-oxoglutarate synergistically with foliar N treatment (DS + N + 2OG) was more beneficial to plant photosynthesis. 2-oxoglutarate significantly enhanced plant N content, glutamine synthetase (GS) and glutamate synthase (GOGAT) activity. Furthermore, 2-oxoglutarate increased the accumulation of proline and soluble sugars under drought stress. Under drought stress, soybean seed yield was increased by DS + N + 2OG treatment by 16.48–17.10% and 14.96–18.84% in 2021 and 2022, respectively. Thus, the combination of foliar N and 2-oxoglutarate better mitigated the adverse effects of drought stress and could better compensate for the yield loss of soybean under drought stress.

期刊: Scientific Reports  2023
作者: Zhijia Gai,Maoming Zhang,Pengfei Zhang,Jingtao Zhang,Jingqi Liu,Lijun Cai,Xü Yang,Na Zhang,Zhengnan Yan,Lei Liu,Guozhong Feng
DOI:10.1038/s41598-023-34403-5

Parental salt priming improves the low temperature tolerance in wheat offspring via modulating the seed proteome

期刊: Plant Science  2022
作者: Lei Liu,Hui Li,Na Li,Shuxin Li,Junhong Guo,Xiangnan Li
DOI:10.1016/j.plantsci.2022.111428

Exogenous application of melatonin improves salt tolerance of sugar beet (Beta vulgaris L.) seedlings

期刊: Acta Physiologiae Plantarum  2022
作者: Lei Liu,Ziyang Wang,Zhijia Gai,Yubo Wang,Bin Wang,Pengfei Zhang,Xinyu Liu,Jingting Chen,Shuyou Zhang,Dan Liu,Chunlei Zou,Caifeng Li
DOI:10.1007/s11738-022-03389-4

Low temperature tolerance is depressed in wild-type and abscisic acid-deficient mutant barley grown in Cd-contaminated soil

期刊: Journal of Hazardous Materials  2022
作者: Lei Liu,Shuxin Li,Junhong Guo,Na Li,Miao Jiang,Xiangnan Li
DOI:10.1016/j.jhazmat.2022.128489

Exogenous Melatonin Reprograms the Rhizosphere Microbial Community to Modulate the Responses of Barley to Drought Stress

The rhizospheric melatonin application-induced drought tolerance has been illuminated in various plant species, while the roles of the rhizosphere microbial community in this process are still unclear. Here, the diversity and functions of the rhizosphere microbial community and related physiological parameters were tested in barley under the rhizospheric melatonin application and drought. Exogenous melatonin improved plant performance under drought via increasing the activities of non-structural carbohydrate metabolism enzymes and activating the antioxidant enzyme systems in barley roots under drought. The 16S/ITS rRNA gene sequencing revealed that drought and melatonin altered the compositions of the microbiome. Exogenous melatonin increased the relative abundance of the bacterial community in carbohydrate and carboxylate degradation, while decreasing the relative abundance in the pathways of fatty acid and lipid degradation and inorganic nutrient metabolism under drought. These results suggest that the effects of melatonin on rhizosphere microbes and nutrient condition need to be considered in its application for crop drought-resistant cultivation.

期刊: International Journal of Molecular Sciences  2022
作者: Fan Ye,Miao Jiang,Peng Zhang,Lei Liu,Shengqun Liu,Chunsheng Zhao,Xiangnan Li
DOI:10.3390/ijms23179665

Foliar application of alpha-ketoglutarate plus nitrogen improves drought resistance in soybean (Glycine max L. Merr.)

AbstractThe aim of the present research was to understand the impacts of foliar nitrogen and α-oxoglutarate on proline accumulation, photosynthesis, and ammonium assimilation of soybean seedlings subjected to drought stress. The data in the present study demonstrated that foliar α-oxoglutarate and nitrogen significantly enhanced leaf glutamine synthetase (GS) activity, glutamate dehydrogenase (GDH) activity, glutamate content, proline content, relative water content (RWC) and photosynthesis of soybean seedlings exposed to drought stress at each stage. Accordingly, the ammonium content was significantly reduced by foliar α-oxoglutarate and nitrogen. These results suggested that a combination of foliar nitrogen plus α-oxoglutarate had an advantage over either foliar nitrogen or foliar α-oxoglutarate in increasing the proline accumulation under drought stress and a combination of foliar nitrogen plus α-oxoglutarate could better mitigate the adverse impacts of drought stress.

期刊: Scientific Reports  2022
作者: Zhijia Gai,Jingqi Liu,Lijun Cai,Jingtao Zhang,Lei Liu
DOI:10.1038/s41598-022-18660-4

Beneficial Effects of Exogenous Melatonin on Overcoming Salt Stress in Sugar Beets (Beta vulgaris L.)

Melatonin has been regarded as a promising substance that enhances the abiotic stress tolerance of plants. However, few studies have devoted attention to the role of melatonin in improving salt tolerance in sugar beets. Here, the effects of different application methods (foliar application (100 μM), root application (100 μM), and combined foliar and root application) of melatonin on the morphological and physiological traits of sugar beets exposed to salt stress were investigated. The results showed that melatonin improved the growth of sugar beet seedlings, root yield and sugar content, synthesis of chlorophyll, photosystem II (PS II) activity, and gas exchange parameters under salt stress conditions. Moreover, melatonin enhanced the capacity of osmotic adjustment by increasing the accumulation of osmolytes (betaine, proline, and soluble sugar). At the same time, melatonin increased the H+-pump activities in the roots, thus promoting Na+ efflux and K+ influx, which maintained K+/Na+ homeostasis and mitigated Na+ toxicity. In addition, melatonin strengthened the antioxidant defense system by enhancing the activities of antioxidant enzymes, modulating the ASA-GSH cycle, and mediating the phenylalanine pathway, which removed superoxide anions (O2•−) and hydrogen peroxide (H2O2) and maintained cell membrane integrity. These positive effects were more pronounced when melatonin was applied by combined foliar and root application. To summarize, this study clarifies the potential roles of melatonin in mitigating salt stress in sugar beets by improving photosynthesis, water status, ion homeostasis, and the antioxidant defense system.

期刊: Plants  2021
作者: Pengfei Zhang,Lei Liu,Xin Wang,Ziyang Wang,He Zhang,Jingting Chen,Xinyu Liu,Yubo Wang,Caifeng Li
DOI:10.3390/plants10050886

Induction of Low Temperature Tolerance in Wheat by Pre-Soaking and Parental Treatment with Melatonin

Low temperatures seriously depress germination and seedling establishment in wheat and it is of great significance to explore approaches to improve wheat tolerance to low temperatures. In this study, the effects of seed pre-soaking and parental treatment with melatonin on seed germination and low temperature tolerance during the early growing stage in wheat were studied. The results showed that pre-soaking with melatonin increased the germination rate, improved antioxidant capacity and accelerated starch degradation under low temperature, which alleviated low temperature-induced damage to the chloroplasts in coleoptiles of wheat seedlings. Parental melatonin treatment during grain filling stage significantly decreased the grain weight. Seeds from parental melatonin-treated plants showed higher germination rates and higher antioxidant enzyme activity than the control seeds under low temperature. In addition, parental treatment with melatonin modulated the activities of carbohydrate metabolism enzymes, which contributes to enhanced low temperature tolerance in wheat offspring. It was suggested that both seed pre-soaking and parental treatment with melatonin could be the effective approaches for low temperature tolerance induction in wheat.

期刊: Molecules  2021
作者: Hua Zhang,Lei Liu,Zongshuai Wang,Guozhong Feng,Qiang Gao,Xiangnan Li
DOI:10.3390/molecules26041192

Long non-coding RNAs in the alkaline stress response in sugar beet (Beta vulgaris L.)

Abstract Background Long noncoding RNAs (lncRNAs) play crucial roles in regulating numerous biological processes in which complicated mechanisms are involved. Nonetheless, little is known about the number, features, sequences, and possible effects of lncRNAs on plant responses to alkaline stress. Results Leaf samples collected based on the control Beta vulgaris L., as well as those under short-term and long-term alkaline treatments, were subjected to high-throughput RNA sequencing, through which a total of 8535 lncRNAs with reliable expression were detected. Of these lncRNAs, 102 and 49 lncRNA expression profiles were altered after short- and long-term alkaline stress, respectively. Moreover, 7 lncRNAs were recognized as precursors to 17 previously identified miRNAs. Four lncRNAs responsive to alkaline stress were estimated as targets for 8 miRNAs. Moreover, computational analysis predicted 4318 potential target genes as lncRNAs responsive to alkaline stress. Analysis of functional annotations showed that the abovementioned possible target genes were involved in various bioprocesses, such as kinase activity, structural constituents of ribosomes, the ribonucleoprotein complex and protein metabolic processes. Association analysis provided convincing proof of the interplay of specific candidate target genes with lncRNAs. Conclusion LncRNAs likely exert vital roles during the regulation of the alkaline stress response and adaptation in plants through interaction with protein-coding genes. The findings of this study contribute to comprehensively examining lncRNAs in Beta vulgaris L. and shed more light on the possible roles and modulating interplays of lncRNAs responsive to alkaline stress, thereby laying a certain basis for functional analyses of these types of Beta vulgaris L. lncRNAs in the future.

期刊: BMC Plant Biology  2020
作者: Chunlei Zou,Yubo Wang,Bin Wang,Dan Liu,Lei Liu,Zhijia Gai,Caifeng Li
DOI:10.1186/s12870-020-02437-w

Beneficial Effects of Biochar-Based Organic Fertilizer on Nitrogen Assimilation, Antioxidant Capacities, and Photosynthesis of Sugar Beet (Beta vulgaris L.) under Saline-Alkaline Stress

The Songnen Plain, whose climatic conditions are perfectly suited to sugar beet growth, is located in northeastern China. Unfortunately, this region has a lot of saline-alkaline land, which is the most important factor limiting sugar beet production. This study was undertaken to determine whether biochar-based organic fertilizer could alleviate the negative effect of saline-alkaline soil on sugar beet yield and whether such an effect correlated with changes in nitrogen assimilation, antioxidant system, root activity, and photosynthesis. Three treatments were established: Chemical fertilizers were applied to neutral soil (CK), chemical fertilizers were applied to saline-alkaline soil (SA), and biochar-based organic fertilizer was applied to saline-alkaline soil (SA + B). Our results showed that saline-alkaline stress significantly inhibited the nitrogen assimilation and antioxidant enzymes activities in root, root activity, and photosynthesis, thus significantly reducing the yield and sugar content of sugar beet. Under saline-alkaline conditions, the application of biochar-based organic fertilizer improved the activities of nitrogen assimilation enzymes in the root; at the same time, the antioxidant enzymes activities of the root were significantly increased for improving root activity in this treatment. Moreover, the application of biochar-based organic fertilizer could improve the synthesis of photosynthetic pigments, PSII (Photosystem II) activity, stomatal opening, and photosynthesis of sugar beet under saline-alkaline conditions. Hence, the growth and yield of sugar beet were improved by applying biochar-based organic fertilizer to saline-alkaline soil. These results proved the significance of biochar-based organic fertilizer in alleviating the negative effect of saline-alkaline stress on sugar beet. The results obtained in the pot experiment may not be viable in field conditions. Therefore, in the future, we will verify whether biochar-based organic fertilizer could alleviate the adverse effects of saline-alkaline stress on sugar beets yield under field conditions.

期刊: Agronomy  2020
作者: Pengfei Zhang,Fangfang Yang,He Zhang,Lei Liu,Xinyu Liu,Jingting Chen,Xin Wang,Yubo Wang,Caifeng Li
DOI:10.3390/agronomy10101562

Exogenous allantoin improves the salt tolerance of sugar beet by increasing putrescine metabolism and antioxidant activities

期刊: Plant Physiology and Biochemistry  2020
作者: Lei Liu,Dan Liu,Ziyang Wang,Chunlei Zou,Bin Wang,He Zhang,Zhijia Gai,Pengfei Zhang,Yubo Wang,Caifeng Li
DOI:10.1016/j.plaphy.2020.06.034

Transcriptomic and metabolomic analyses reveal mechanisms of adaptation to salinity in which carbon and nitrogen metabolism is altered in sugar beet roots

AbstractBackgroundBeta vulgarisL. is one of the main sugar-producing crop species and is highly adaptable to saline soil. This study explored the alterations to the carbon and nitrogen metabolism mechanisms enabling the roots of sugar beet seedlings to adapt to salinity.ResultsThe ionome, metabolome, and transcriptome of the roots of sugar beet seedlings were evaluated after 1 day (short term) and 7 days (long term) of 300 mM Na+treatment. Salt stress caused reactive oxygen species (ROS) damage and ion toxicity in the roots. Interestingly, under salt stress, the increase in the Na+/K+ratio compared to the control ratio on day 7 was lower than that on day 1 in the roots. The transcriptomic results showed that a large number of differentially expressed genes (DEGs) were enriched in various metabolic pathways. A total of 1279 and 903 DEGs were identified on days 1 and 7, respectively, and were mapped mainly to 10 Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways. Most of the genes were involved in carbon metabolism and amino acid (AA) biosynthesis. Furthermore, metabolomic analysis revealed that sucrose metabolism and the activity of the tricarboxylic acid (TCA) cycle increased in response to salt stress. After 1 day of stress, the content of sucrose decreased, whereas the content of organic acids (OAs) such as L-malic acid and 2-oxoglutaric acid increased. After 7 days of salt stress, nitrogen-containing metabolites such as AAs, betaine, melatonin, and (S)-2-aminobutyric acid increased significantly. In addition, multiomic analysis revealed that the expression of the gene encoding xanthine dehydrogenase (XDH) was upregulated and that the expression of the gene encoding allantoinase (ALN) was significantly downregulated, resulting in a large accumulation of allantoin. Correlation analysis revealed that most genes were significantly related to only allantoin and xanthosine.ConclusionsOur study demonstrated that carbon and nitrogen metabolism was altered in the roots of sugar beet plants under salt stress. Nitrogen metabolism plays a major role in the late stages of salt stress. Allantoin, which is involved in the purine metabolic pathway, may be a key regulator of sugar beet salt tolerance.

期刊: BMC Plant Biology  2020
作者: Lei Liu,Bin Wang,Dan Liu,Chunlei Zou,Peiran Wu,Ziyang Wang,Yubo Wang,Caifeng Li
DOI:10.1186/s12870-020-02349-9

Effects of exogenous α-oxoglutarate on proline accumulation, ammonium assimilation and photosynthesis of soybean seedling (Glycine max(L.) Merr.) exposed to cold stress

AbstractThe objective of this study was to examine the effects of exogenous α-oxoglutarate on leaf proline accumulation, ammonium assimilation and photosynthesis of soybean when exposed to cold stress. To achieve this objective, exogenous α-oxoglutarate was sprayed to potted seedlings of Henong60 and Heinong48 at 0, 2.5, 5.0 and 7.5 mmol/L, identified as A0, A2.5, A5.0, and A7.5, respectively. Leaf samples were collected after cold stress of 24 h (S1 stage) and 48 h (S2 stage). The results indicated that exogenous α-oxoglutarate significantly enhanced leaf GS activity, NADP-GDH activity, glutamate content, proline content and photosynthesis of soybean seedling exposed to cold stress at S1 and S2 stages. The ammonium content in leaf was significantly decreased by exogenous α-oxoglutarate at both stages. 5.0 mmol/L of exogenous α-oxoglutarate is the optimum concentration in this study. Leaf proline content for Henong60 and Heinong48 at A5.0 was 37.53% and 17.96% higher than that at A0 at S1 stage, respectively. Proline content for Henong60 and Heinong48 increased by 28.82% and 12.41% at A5.0 and A0, respectively, at S2 stage. Those results suggested that exogenous α-oxoglutarate could alleviate the adverse effects of cold stress.

期刊: Scientific Reports  2020
作者: Zhijia Gai,Lei Liu,Jingtao Zhang,Jingqi Liu,Lijun Cai
DOI:10.1038/s41598-020-74094-w

Transcriptome analysis of sugar beet (Beta vulgaris L.) in response to alkaline stress

期刊: Plant Molecular Biology  2020
作者: Chunlei Zou,Dan Liu,Peiran Wu,Yubo Wang,Zhijia Gai,Lei Liu,Fangfang Yang,Caifeng Li,Guanghao Guo
DOI:10.1007/s11103-020-00971-7

Responses of Soil Microorganisms and Enzymatic Activities to Alkaline Stress in Sugar Beet Rhizosphere

期刊: Polish Journal of Environmental Studies  2019
作者: Lei Liu,Yubo Wang,Zhijia Gai,Dan Liu,Peiran Wu,Bin Wang,Chunlei Zou,Caifeng Li,Fangfang Yang
DOI:10.15244/pjoes/105244

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