Plant resistance inducer AMHA enhances antioxidant capacities to promote cold tolerance by regulating the upgrade of glutathione S-transferase in tea plant

Xuejin Chen , Ning Zhou , Lisha Yu , Zhaolan Han , Yanjing Guo , Salome Njeri Ndombi , Huan Zhang , Jie Jiang , Yu Duan , Zhongwei Zou , Yuanchun Ma , Xujun Zhu , Shiguo Chen , Wanping Fang

Horticulture Research ›› 2025, Vol. 12 ›› Issue (6) : 73

PDF (5070KB)
Horticulture Research ›› 2025, Vol. 12 ›› Issue (6) :73 DOI: 10.1093/hr/uhaf073
Articles
research-article
Plant resistance inducer AMHA enhances antioxidant capacities to promote cold tolerance by regulating the upgrade of glutathione S-transferase in tea plant
Author information +
History +
PDF (5070KB)

Abstract

Plant resistance inducers represent an alternative strategy that mitigate stress-induced damage in plants. Previously, 2-amino-3-methylhexanoic acid (AMHA), a novel natural plant resistance inducer, was shown to significantly bolster cold tolerance, thermotolerance, and pathogen resistance in plants. However, the intricate mechanisms underlying AMHA’s response to cold stress remain elusive. Thus, we investigated the physiological and transcriptomic analyses of AMHA pretreatment on tea plant to determine its substantial role of AMHA under cold stress. The results showed that pretreatment with 100 nM AMHA effectively mitigated the detrimental effects of cold stress on photosynthesis and growth. Furthermore, differentially expressed genes were identified through RNA-seq during pretreatment, cold stress, and 2 days of recovery. These genes were mainly enriched in pathways related to flavonoid/anthocyanin, carotenoid, and ascorbic acid-glutathione (AsA-GSH) cycle, including GST (encoding glutathione S-transferase). Potential regulatory relationships between the identified genes and transcription factors were also established. Antisense oligodeoxynucleotide-silencing and overexpression experiments revealed that CsGSTU7 enhances cold resistance by maintaining redox homeostasis. In conclusion, our study suggests that antioxidant-related signaling molecules play a critical role in the signaling cascades and transcriptional regulation mediating AMHA-induced cold-stress resistance in tea plant.

Cite this article

Download citation ▾
Xuejin Chen, Ning Zhou, Lisha Yu, Zhaolan Han, Yanjing Guo, Salome Njeri Ndombi, Huan Zhang, Jie Jiang, Yu Duan, Zhongwei Zou, Yuanchun Ma, Xujun Zhu, Shiguo Chen, Wanping Fang. Plant resistance inducer AMHA enhances antioxidant capacities to promote cold tolerance by regulating the upgrade of glutathione S-transferase in tea plant. Horticulture Research, 2025, 12(6): 73 DOI:10.1093/hr/uhaf073

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was supported by the National Key R&D Program of China (2023YFD17006000), Major science and technology projects in Yunnan Province (202402AE090015), National Natural Science Foundation of China (32160729), China Agriculture Research System of MOF and MARA (CARS-19), Hainan Nongken Investment Holding Group Co., Ltd (HKKJ202426), and Suzhou science and technology project (SNG2023001), and Postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX24_0963).

Author contributions

W.F., S.C., and X.C. conceived the ideas and designed the methodology. X.C., N.Z., L.Y., Z.H., Y.G., and H.Z. performed the experiments. X.C., S.C., X.Z., J.J., Y.D., and Y. M. analyzed the data and wrote the draft. S.C., W.F., Z.Z., X. Z., and S.N.N. revised the manuscript. All authors read the manuscript.

Data availability

All relevant data in this study were provided in the article and its supplementary files. The raw sequences of RNA-seq were submitted to the NCBI Sequence Read Archive under BioProject accession number PRJCA003382.

Conflict of interest statement

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.

Supplementary Data

Supplementary data is available at Horticulture Research online.

References

[1]

Guo X, Liu D, Chong K. Cold signaling in plants: insights into mechanisms and regulation. J Integr Plant Biol. 2018; 60:745-56

[2]

Kidokoro S, Shinozaki K, Yamaguchi-Shinozaki K. Transcrip-tional regulatory network of plant cold-stress responses. Trends Plant Sci. 2022; 27:922-35

[3]

Li X, Ahammed GJ, Li Z. et al. Freezing stress deteriorates tea quality of new flush by inducing photosynthetic inhibition and oxidative stress in mature leaves. Sci Hortic. 2017; 230:155-60

[4]

Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem. 2010; 48:909-30

[5]

Ron Mittler SIZ, Fichman Y, Van Breusegem. Reactive oxygen species signalling in plant stress responses. Nat Rev Mol Cell Biol. 2022; 23:663-79

[6]

Hasanuzzaman M, Bhuyan M, Anee TI. et al. Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants (Basel). 2019; 8:384

[7]

Xu Z, Wang J, Ma Y. et al. The bZIP transcription factor SlAREB1 regulates anthocyanin biosynthesis in response to low temper-ature in tomato. Plant J. 2023; 115:205-19

[8]

Wang Y, Chen F, Ma Y. et al. An ancient whole-genome duplica-tion event and its contribution to flavor compounds in the tea plant (Camellia sinensis). Hortic Res. 2021; 8:176

[9]

Xia E, Zhang H, Sheng J. et al. The tea tree genome provides insights into tea flavor and independent evolution of caffeine biosynthesis. Mol Plant. 2017; 10:866-77

[10]

Yang Q, Guo Y, Li J. et al. Natural plant inducer 2-amino-3-methylhexanoic acid protects physiological activity against high-temperature damage to tea (Camellia sinensis). Sci Hortic. 2023; 312:111836

[11]

Wang P, Jin S, Chen X. et al. Chromatin accessibility and transla-tional landscapes of tea plants under chilling stress. Hortic Res. 2021; 8:1458-72

[12]

Zhao HM, Li AI, Li F. et al. Characterization of CsWRKY29 and CsWRKY37 transcription factors and their functional roles in cold tolerance of tea plant. Beverage Plant Res. 2022; 2:1-13

[13]

Yan Y, Jeong S, Park CE. et al. Effects of extreme temperature on China’s tea production. Environ Res Lett. 2021; 16:044040

[14]

Li Y, Zhang Q, Ou L. et al. Response to the cold stress signaling of the tea plant (Camellia sinensis) elicited by chitosan oligosac-charide. Agronomy. 2020; 10:915

[15]

Zhang Y, Ming R, Khan M. et al. ERF9 of Poncirus trifoliata (L.) Raf. Undergoes feedback regulation by ethylene and modulates cold tolerance via regulating a glutathione S-transferase U17 gene. Plant Biotechnol J. 2022; 20:183-200

[16]

Han Z, Zhang C, Zhang H. et al. CsMYB transcription factors participate in jasmonic acid signal transduction in response to cold stress in tea plant (Camellia sinensis). Plants (Basel). 2022; 11:2869

[17]

Mao K, Li J, Wu S. et al. Melatonin treatment promotes cold adaptation and spring growth of tea plants. IndCropProd. 2023; 200:116834

[18]

Han ZZ, Li H, Duan P. et al. Genome-wide characterization and identification of candidate CsRAV genes involved in JA pathway responses to cold stress in tea plant (Camellia sinensis). Beverage Plant Res. 2023; 3:0

[19]

De Kesel J, Conrath U, Flors V. et al. The induced resistance lexicon: Do’s and don’ts. Trends Plant Sci. 2021; 26:685-91

[20]

Baltazar M, Correia S, Guinan KJ. et al. Recent advances in the molecular effects of biostimulants in plants: an overview. Biomol Ther. 2021; 11:1096

[21]

García-García AL, García-Machado FJ, Borges AA. et al. Pure organic active compounds against abiotic stress: a biostimulant overview. Front Plant Sci. 2020; 11:575829

[22]

Li X, Wei J, Scott E. et al. Exogenous melatonin alleviates cold stress by promoting antioxidant defense and redox homeostasis in Camellia sinensis L. Molecules. 2018; 23:165

[23]

Zhu X, Liao J, Xia X. et al. Physiological and iTRAQ-based proteomic analyses reveal the function of exogenous γ-aminobutyric acid (GABA) in improving tea plant (Camellia sinensis L.) tolerance at cold temperature. BMC Plant Biol. 2019; 19:43

[24]

YanF, QuD, ChenX. et al. Metabolomics reveals 5-aminolevulinic acid improved the ability of tea leaves (Camellia sinensis L.) against cold stress. Meta. 2022; 12:392

[25]

Wang T, Duan Y, Liu G. et al. Tea plantation intercropping green manure enhances soil functional microbial abundance and multifunctionality resistance to drying-rewetting cycles. Sci Total Environ. 2022; 810:151282

[26]

Strasser RJ, Tsimilli-Michael M, Srivastava A. Analysis of the chlorophyll a fluorescence transient. In: In Chlorophyll Fluo-rescence:A Signature of Photosynthesis. Springer Netherlands: Dordrecht, 2004;321-62

[27]

Cejudo FJ, Sandalio LM, Van Breusegem F. Understanding plant responses to stress conditions: redox-based strategies. JExp Bot. 2021; 72:5785-8

[28]

Mi X, Tang M, Zhu J. et al. Alternative splicing of CsWRKY21 positively regulates cold response in tea plant. Plant Physiol Biochem. 2024; 208:108473

[29]

Ding CH, Wang X, Li L. et al. iTRAQ-based quantitative proteomic analysis of tea plant (Camellia sinensis (L.) O. Kuntze) during cold acclimation and de-acclimation procedures. Beverage Plant Res. 2023; 3:0

[30]

Wang H, Liu Z, Luo S. et al. 5-aminolevulinic acid and hydrogen sulphide alleviate chilling stress in pepper (Capsicum annuum L.) seedlings by enhancing chlorophyll synthesis pathway. Plant Physiol Biochem. 2021; 167:567-76

[31]

Bodin E, Bellée A, Dufour MC. et al. Grapevine stimulation: a multidisciplinary approach to investigate the effects of biostim-ulants and a plant defense stimulator. J Agric Food Chem. 2020; 68: 15085-96

[32]

Wei Y, Chen H, Wang L. et al. Cold acclimation alleviates cold stress-induced PSII inhibition and oxidative damage in tobacco leaves. Plant Signal Behav. 2022; 17:2013638

[33]

Duan X, Yu X, Wang Y. et al. Genome-wide identification and expression analysis of glutathione S-transferase gene family to reveal their role in cold stress response in cucumber. Front Genet. 2022; 13:1009883

[34]

Hu Z, Fan J, Xie Y. et al. Comparative photosynthetic and metabolic analyses reveal mechanism of improved cold stress tolerance in bermudagrass by exogenous melatonin. Plant Physiol Biochem. 2016; 100:94-104

[35]

Guo Y, Liu W, Wang H. et al. Action mode of the mycotoxin patulin as a novel natural photosystem II inhibitor. J Agric Food Chem. 2021; 69:7313-23

[36]

Ashrostaghi T, Aliniaeifard S, Shomali A. et al. Light intensity: the role player in cucumber response to cold stress. Agronomy. 2022; 12:201

[37]

Jin J, Zhao M, Jing T. et al. (Z)-3-hexenol integrates drought and cold stress signaling by activating abscisic acid glucosylation in tea plants. Plant Physiol. 2023; 193:1491-507

[38]

Smirnoff N. Ascorbic acid: metabolism and functions of a multi-facetted molecule. Curr Opin Plant Biol. 2000; 3:229-35

[39]

Fan L, Ding T, Zuo J. et al. Amelioration of postharvest chilling injury in sweet pepper by glycine betaine. Postharvest Biol Technol. 2016; 112:114-20

[40]

Li Y, Chu Z, Luo J. et al. The C2H2 zinc-finger protein SlZF3 regulates AsA synthesis and salt tolerance by interacting with CSN5B. Plant Biotechnol J. 2018; 16:1201-13

[41]

Liu X, Bulley SM, Varkonyi-Gasic E. et al. Kiwifruit bZIP transcrip-tion factor AcePosF21 elicits ascorbic acid biosynthesis during cold stress. Plant Physiol. 2023; 192:982-99

[42]

Zhang X, Li L, He Y. et al. The CsHSFA-CsJAZ6 module-mediated high temperature regulates flavonoid metabolism in Camellia sinensis. Plant Cell Environ. 2023; 46:2401-18

[43]

Chen X, Wang P, Gu M. et al. Identification of PAL genes related to anthocyanin synthesis in tea plants and its correlation with anthocyanin content. Hortic Plant J. 2022; 8:381-94

[44]

Song Z, Lai X, Chen H. et al. Role of MaABI5-like in abscisic acid-induced cold tolerance of ’Fenjiao’ banana fruit. Hortic Res. 2022;9:uhac130

[45]

Wang L, Di T, Peng J. et al. Comparative metabolomic analysis reveals the involvement of catechins in adaptation mechanism to cold stress in tea plant (Camellia sinensis var. sinensis). Environ Exp Bot. 2022; 201:104978

[46]

Hao X, Tang H, Wang B. et al. Integrative transcriptional and metabolic analyses provide insights into cold spell response mechanisms in young shoots of the tea plant. Tree Physiol. 2018; 38:1655-71

[47]

Nisar N, Li L, Lu S. et al. Carotenoid metabolism in plants. Mol Plant. 2015; 8:68-82

[48]

Wurtzel ET. Changing form and function through carotenoids and synthetic biology. Plant Physiol. 2019; 179:830-43

[49]

Cheng X, Sun Y, Wang Y. et al. CsCBF2 contributes to cold repression of chlorophyll and carotenoid biosynthesis in albino Camellia sinensis cv. Baiye 1. Tree Physiol. 2024; 44:149

[50]

Ding Y, Yang S. Surviving and thriving: how plants perceive and respond to temperature stress. Dev Cell. 2022; 57:947-58

[51]

Wang H, Li J, Yang Q. et al. Natural 2-amino-3-methylhexanoic acid as plant elicitor inducing resistance against temperature stress and pathogen attack. Int J Mol Sci. 2022; 23:5715

[52]

Wang P, Liu WC, Han C. et al. Reactive oxygen species: multidi-mensional regulators of plant adaptation to abiotic stress and development. J Integr Plant Biol. 2024; 66:330-67

[53]

Dietz KJ, Turkan I, Krieger-Liszkay A. Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesiz-ing chloroplast. Plant Physiol. 2016; 171:1541-50

[54]

Foyer CH, Hanke G. ROS production and signalling in chloro-plasts: cornerstones and evolving concepts. Plant J. 2022; 111: 642-61

[55]

Han X, Yang Z, Liu Y. et al. Genome-wide profiling of expres-sion and biochemical functions of the Medicago glutathione S-transferase gene family. Plant Physiol Biochem. 2018; 126: 126-33

[56]

Lu C, Zhang P, Li S. et al. Isolation and characterization of glu-tathione S-transferase genes and their transcripts in Saccharina japonica (Laminariales, Phaeophyceae) during development and under abiotic stress. BMC Plant Biol. 2023; 23:436

[57]

Ding F, Wang C, Zhang S. et al. A jasmonate-responsive glutathione S-transferase gene SlGSTU24 mitigates cold-induced oxidative stress in tomato plants. Sci Hortic. 2022; 303: 111231

[58]

CaoQ, LvW, JiangH. et al. Genome-wide identification of glutathione S-transferase gene family members in tea plant (Camellia sinensis) and their response to environmental stress. Int J Biol Macromol. 2022; 205:749-60

[59]

Manuel UJ, Liliana L, Ariel H-V. et al. A dual role for glu-tathione transferase U7 in plant growth and protection from methyl viologen-induced oxidative stress. Plant Physiol. 2021; 187: 2451-68

[60]

Di T, Wu Y, Feng X. et al. CIPK11 phosphorylates GSTU23 to promote cold tolerance in Camellia sinensis. Plant Cell Environ. 2024; 47:4786-99

[61]

Basantani M, Srivastava A. Plant glutathione transferases - a decade falls short. Can J Bot. 2011; 85:443-56

[62]

Ye Q, Zheng L, Liu P. et al. The S-acylation cycle of transcription factor MtNAC80 influences cold stress responses in Medicago truncatula. Plant Cell. 2024; 36:2629-51

[63]

Chen S, Yang J, Zhang M. et al. Classification and characteristics of heat tolerance in Ageratina adenophora populations using fast chlorophyll a fluorescence rise OJIP. Environ Exp Bot. 2016; 122: 126-40

[64]

Shen J, Zou Z, Zhang X. et al. Metabolic analyses reveal different mechanisms of leaf color change in two purple-leaf tea plant (Camellia sinensis L.) cultivars. Hortic Res. 2018; 5:7

[65]

Cao Y, Chen Y, Cheng N. et al. CsCuAO 1 associated with CsAMADH1 confers drought tolerance by modulating GABA levels in tea plants. Int J Mol Sci. 2024; 25:992

[66]

Zhao M, Cai B, Jin J. et al. Cold stress-induced glucosyltransferase CsUGT78A15 is involved in the formation of eugenol glucoside in Camellia sinensis. Hortic Plant J. 2020; 6:439-49

[67]

Zhang T, Xiao J, Zhao Y. et al. Comparative physiological and transcriptomic analyses reveal ascorbate and glutathione coreg-ulation of cadmium toxicity resistance in wheat genotypes. BMC Plant Biol. 2021; 21:459

[68]

Shen J, Zhang D, Zhou L. et al. Transcriptomic and metabolomic profiling of Camellia sinensis L. cv. ’Suchazao’ exposed to tem-perature stresses reveals modification in protein synthesis and photosynthetic and anthocyanin biosynthetic pathways. Tree Physiol. 2019; 39:1583-99

[69]

Lei X, Wang Y, Zhou Y. et al. TeaPGDB: tea plant genome database. Beverage Plant Res. 2021; 1:1-12

[70]

Wang PJ,YuJX,JinS. et al. Genetic basis of high aroma and stress tolerance in the oolong tea cultivar genome. Hortic Res. 2021; 8:107

[71]

Shannon P. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003; 13:2498-504

[72]

Chen C, Chen H, Zhang Y. et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020; 13:1194-202

PDF (5070KB)

297

Accesses

0

Citation

Detail

Sections
Recommended

/