Enhancing tomato fruit antioxidant potential through hydrogen nanobubble irrigation

Abstract

Eating fruits and vegetables loaded with natural antioxidants can boost human health considerably and help fight off diseases linked to oxidative stress. Hydrogen has unique antioxidant effects. However, its low-solubility and fast-diffusion has limited its applications in agriculture. Integration of hydrogen with nanobubble technology could address such problems. However, the physiological adaptation and response mechanism of crops to hydrogen nanobubbles is still poorly understood. Antioxidant concentrations of lycopene, ascorbic acid, flavonoids, and resveratrol in hydrogen nanobubble water drip-irrigated tomato fruits increased by 16.3-264.8% and 2.2-19.8%, respectively, compared to underground water and oxygen nanobubble water. Transcriptomic and metabolomic analyses were combined to investigate the regulatory mechanisms that differed from the controls. Comprehensive multi-omics analysis revealed differences in the abundances of genes responsible for hormonal control, hydrogenase genes, and necessary synthetic metabolites of antioxidants, which helped to clarify the observed improvements in antioxidants. This is the first case of hydrogen nanobubble water irrigation increasing numerous natural antioxidant parts in fruits. Considering the characteristics of hydrogen and the application of the nanobubble technology in agriculture, the findings of the present study could facilitate the understanding of the potential effects of hydrogen on biological processes and the mechanisms of action on plant growth and development.

Acknowledgements

This study was financially supported by the Major Program of National Natural Science Foundation of China (52339004) and National Natural Science Foundation of China (51979274 and 52109070). We thank the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) for funding: Projektnummer 471624304. We thank Dr David Midmore for language editing, Dr Sergi Munné-Bosch for recommending and guiding the advanced experimental methods, Abidur Rahman for suggesting transcriptome testing and hormone results validation. We thank Majorbio for providing the platform for gene sequencing, metabolite identification, and Majorbio Cloud Platform. We thank Shanghai Yuanye Bio-Technology Co., Ltd and Beijing Solarbio Science & Technology Co., Ltd for providing test kits for enzyme activity and radical scavenging capacity to assay antioxidant capacity of tomatoes.

Author contributions

Y.L. conceived and designed the research. J.H. conducted the experiments, analysed the data, and wrote the paper. Y.L. and Y.Z. gave guidance on the paper structure and picture design. Y.Z. and C.-M.G. checked and enhanced the grammar and descriptions, and improved paragraph coherence and enriched data. J.C. guided on the methodology during the experiments, and then checked and modified the description of the Materials and Methods of the paper. D.F. provided a prominent contribution on the pictures’ details and multiomics professional expression. S.B. meticulously checked and revised the descriptions of the results and graphical details. Y.L. and Y.L. discussed the results and commented on the manuscript.

Data availability

The data that support the findings of this study are available in the Supporting Information of this article. The fastq sequence data with associated metadata for this study have been deposited at the National Center for Biotechnology Information (NCBI) under BioProject PRJNA119.

Conflict of interest statement

The authors declare no competing financial interests that are of commercial interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1] Mansoor S, Ali Wani O, Lone JK. et al. Reactive oxygen species in plants: from source to sink. Antioxidants. 2022; 11:225

[2] Farooq MA, Niazi AK, Akhtar J. et al. Acquiring control: the evolution of ROS-induced oxidative stress and redox signaling pathways in plant stress responses. Plant Physiol Biochem. 2019; 141:353-69

[3] Mittler R, Zandalinas SI, Fichman Y. et al. Reactive oxygen species signalling in plant stress responses. Nat Rev Mol Cell Biol. 2022; 23:663-79

[4] Yong KT, Yong PH, Ng ZX. Tomato and human health: a perspective from post-harvest processing, nutrient bio-accessibility, and pharmacological interaction. Food Frontiers. 2023; 4:1702-19

[5] Key T. Fruit and vegetables and cancer risk. Br J Cancer. 2011; 104:6-11

[6] WHO. Fruit and Vegetables for Health: Report of the Joint FAO. Japan: World Health Organization, 2005

[7] Jian S, Yang K, Zhang L. et al. The modulation effects of plant-derived bioactive ingredients on chronic kidney disease: focus on the gut-kidney axis. Food Frontiers. 2023; 4:262-82

[8] Barbagallo RN, Di Silvestro I, Patanè C. Yield, physicochemical traits, antioxidant pattern, polyphenol oxidase activity and total visual quality of field-grown processing tomato cv. Brigade as affected by water stress in Mediterranean climate. J Sci Food Agric. 2013; 93:1449-57

[9] Muzolf-Panek M, Kleiber T, Kaczmarek A. Effect of increasing manganese concentration in nutrient solution on the antioxidant activity, vitamin C, lycopene and polyphenol contents of tomato fruit. Food Addit Contam Part A. 2017; 34:379-89

[10] Seneviratne G, Jayakody K, Weerasekara M. et al. Microbial biofertilizer application versus compost use in agriculture: soil health implications. Soil Environ Health. 2011; 4:81-117

[11] Kaur G, Asthir B. Molecular responses to drought stress in plants. Biol Plant. 2017; 61:201-9

[12] Li L, Wang J, Jiang K. et al. Preharvest application of hydrogen nanobubble water enhances strawberry flavor and consumer preferences. Food Chem. 2022; 377:131953

[13] Wang Y, Wang S, Sun J. et al. Nanobubbles promote nutrient utilization and plant growth in rice by upregulating nutrient uptake genes and stimulating growth hormone production. Sci Total Environ. 2021; 800:149627

[14] Zhang Y, Fan W, Li X. et al. Enhanced removal of free radicals by aqueous hydrogen nanobubbles and their role in oxidative stress. Environ Sci Technol. 2022; 56:15096-107

[15] Hu H, Li P, Wang Y. et al. Hydrogen-rich water delays postharvest ripening and senescence of kiwifruit. Food Chem. 2014; 156:100-9

[16] Xu S, Zhu S, Jiang Y. et al. Hydrogen-rich water alleviates salt stress in rice during seed germination. Plant Soil. 2013; 370:47-57

[17] Zhao L, Teng M, Zhou L. et al. Hydrogen nanobubble water: a good assistant for improving the water environment and agricultural production. J Agric Food Chem. 2023; 71:12369-71

[18] Temesgen T, Bui TT, Han M. et al. Micro and nanobubble technologies as a new horizon for water-treatment techniques: a review. Adv Colloid Interf Sci. 2017; 246:40-51

[19] Liu Y, Zhou Y, Wang T. et al. Micro-nano bubble water oxygation: synergistically improving irrigation water use efficiency, crop yield and quality. J Clean Prod. 2019; 222:835-43

[20] Xue S, Marhaba T, Zhang W. Nanobubble watering affects nutrient release and soil characteristics. ACS Agric Sci Tech. 2022; 2:453-61

[21] Liu S, Li J, Oshita S. et al. Formation of a hydrogen radical in hydrogen nanobubble water and its effect on copper toxicity in Chlorella. ACS Sustain Chem Eng. 2021; 9:11100-9

[22] Yan D, Xue S, Zhang Z. et al. Air nanobubble water improves plant uptake and tolerance toward cadmium in phytoremediation. Environ Pollut. 2023; 337:122577

[23] Leroy V, Norisuye T. Investigating the existence of bulk nanobubbles with ultrasound. Chem Phys Chem. 2016; 17:2787-90

[24] Tanaka K, Gilroy S, Jones AM. et al. Extracellular ATP signaling in plants. Trends Cell Biol. 2010; 20:601-8

[25] Liu S, Oshita S, Makino Y. et al. Oxidative capacity of nanobubbles and its effect on seed germination. ACS Sustain Chem Eng. 2016; 4:1347-53

[26] Liu S, Oshita S, Thuyet DQ. et al. Antioxidant activity of hydrogen nanobubbles in water with different reactive oxygen species both in vivo and in vitro. Langmuir. 2018; 34:11878-85

[27] Maia J, Dekkers BJ, Dolle MJ. et al. Abscisic acid (ABA) sensitivity regulates desiccation tolerance in germinated Arabidopsis seeds. New Phytol. 2014; 203:81-93

[28] Marslin G, Sheeba CJ, Franklin G. Nanoparticles alter secondary metabolism in plants via ROS burst. Front Plant Sci. 2017; 8:832

[29] Martin RE, Postiglione AE, Muday GK. Reactive oxygen species function as signaling molecules in controlling plant development and hormonal responses. Curr Opin Plant Biol. 2022; 69:102293

[30] Miralles P, Church TL, Harris AT. Toxicity, uptake, and translocation of engineered nanomaterials in vascular plants. Environ Sci Technol. 2012; 46:9224-39

[31] Mittler R. ROS are good. Trends Plant Sci. 2017; 22:11-9

[32] Mittler R, Blumwald E. The roles of ROS and ABA in systemic acquired acclimation. Plant Cell. 2015; 27:64-70

[33] Mittler R, Vanderauwera S, Gollery M. et al. Reactive oxygen gene network of plants. Trends Plant Sci. 2004; 9:490-8

[34] Moore BD, Andrew RL, Külheim C. et al. Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol. 2014; 201:733-50

[35] Parisi C, Vigani M, Rodríguez-Cerezo E. Agricultural nanotechnologies: what are the current possibilities? Nano Today. 2015; 10:124-7

[36] Pitzschke A, Forzani C, Hirt H. Reactive oxygen species signaling in plants. Antioxid Redox Signal. 2006; 8:1757-64

[37] Resnick JS, Wen C-K, Shockey JA. et al. Reversion-to-ethylene sensitivity1, a conserved gene that regulates ethylene receptor function in Arabidopsis. Proc Natl Acad Sci. 2006; 103:7917-22

[38] Rico CM, Majumdar S, Duarte-Gardea M. et al. Interaction of nanoparticles with edible plants and their possible implications in the food chain. J Agric Food Chem. 2011; 59:3485-98

[39] Sies H, Berndt C, Jones DP. Oxidative stress. Annu Rev Biochem. 2017; 86:715-48

[40] Song Y, Zhai Y, Li L. et al. BIN2 negatively regulates plant defence against Verticillium dahliae in Arabidopsis and cotton. Plant Biotechnol J. 2021; 19:2097-112

[41] Berghe TV, Linkermann A, Jouan-Lanhouet S. et al. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat Rev Mol Cell Biol. 2014; 15:135-47

[42] Denness L, McKenna JF, Segonzac C. et al. Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiol. 2011; 156:1364-74

[43] Hartman S, Sasidharan R, Voesenek LA. The role of ethylene in metabolic acclimations to low oxygen. New Phytol. 2021; 229:64-70

[44] Hayes JD, Dinkova-Kostova AT, Tew KD. Oxidative stress in cancer. Cancer Cell. 2020; 38:167-97

[45] Kyzas GZ, Mitropoulos AC. From bubbles to nanobubbles. Nano. 2021; 11:2592

[46] Wang F, Chen B, Yan B. et al. Scattered light imaging enables real-time monitoring of label-free nanoparticles and fluorescent biomolecules in live cells. J Am Chem Soc. 2019; 141:14043-7

[47] Xue S, Gao J, Liu C. et al. Unveiling the potential of nanobubbles in water: impacts on tomato’s early growth and soil properties. Sci Total Environ. 2023; 903:166499

[48] Agarwal A, Ng WJ, Liu Y. Principle and applications of microbubble and nanobubble technology for water treatment. Chemosphere. 2011; 84:1175-80

[49] Atkinson AJ, Apul OG, Schneider O. et al. Nanobubble technologies offer opportunities to improve water treatment. Accounts Chem Res. 2019; 52:1196-205