Abstract
To meet the increasing demands for higher-value and nutrient-rich vegetables, this work aims to investigate whether molecular hydrogen (H2)-based irrigation, in the form of hydrogen nanobubble water (HNW), could improve yield and quality of Chinese cabbage (Brassica chinensis L.). Field trials showed that compared to surface water (SW) irrigation (control group), HNW irrigation significantly increased Chinese cabbage yield by 32.70 ± 12.15%, and the single plant weight, height, the maximum leaf length and width were also significantly increased. Higher nutritional value, including the increased contents of soluble sugar, soluble protein, mineral nutrients (P, Fe, Zn, and Cu), and secondary metabolites (total carotenoids, proanthocyanidins, phenols, flavonoids, and ascorbic acid), as well as decreased nitrate content and higher antioxidant capability (assessed by DPPH, ABTS and FRAP values) were also observed. Molecular evidence further revealed that the expressions of genes related to Fe, Zn, and P absorption as well as ascorbic acid biosynthesis were obviously up-regulated, consistent with changes in Fe, Zn, P, and ascorbic acid accumulation achieved after HNW irrigation. These results clearly suggested that HNW might have a practical value in improving yield and quality of horticultural crops.
References
Ahmad A, Baig AA, Hussain M et al (2022) Narrative on hydrogen therapy and its clinical applications: safety and efficacy. Curr Pharm Des 28:2519–2537. https://doi.org/10.2174/1381612828666220728104200
An H, Qi X, Gaynor ML et al (2019) Transcriptome and organellar sequencing highlights the complex origin and diversification of allotetraploid Brassica napus. Nat Commun 10:2878. https://doi.org/10.1038/s41467-019-10757-1
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Plant Biol Ann Rev 50:601–639. https://doi.org/10.1146/annurev.arplant.50.1.601
Cao ZY, Duan XL, Yao P et al (2017) Hydrogen gas is involved in auxin-induced lateral root formation by modulating nitric oxide synthesis. Int J Mol Sci 18:2084. https://doi.org/10.3390/ijms18102084
Chen ZP, Xie YJ, Gu Q et al (2017) The AtrbohF-dependent regulation of ROS signaling is required for melatonin-induced salinity tolerance in Arabidopsis. Free Radical Biol Med 108:465–477. https://doi.org/10.1016/j.freeradbiomed.2017.04.009
Cheng PF, Wang J, Zhao ZS et al (2021) Molecular hydrogen increases quantitative and qualitative traits of rice grain in field trials. Plants 10:2331. https://doi.org/10.3390/plants10112331
Cheng PF, Wang YQ, Cai CX et al (2023) Molecular hydrogen positively regulates nitrate uptake and seed size by targeting nitrate reductase. Plant Physiol. https://doi.org/10.1093/plphys/kiad474
Dai C, Cui WT, Pan J et al (2017) Proteomic analysis provides insights into the molecular bases of hydrogen gas-induced cadmium resistance in Medicago sativa. J Proteom 152:109–120. https://doi.org/10.1016/j.jprot.2016.10.013
DiDonato RJ Jr, Roberts LA, Sanderson T et al (2004) Arabidopsis Yellow Stripe-Like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J 39:403–414. https://doi.org/10.1111/j.1365-313X.2004.02128.x
Drouin G, Godin JR, Pagé B (2011) The genetics of vitamin C loss in vertebrates. Curr Genom 12:371–378. https://doi.org/10.2174/138920211796429736
Duan PG, Rao YC, Zeng D et al (2014) SMALL GRAIN 1, which encodes a mitogenactivated protein kinase kinase 4, influences grain size in rice. Plant J 77:547–557. https://doi.org/10.1111/tpj.12405
Fan WH, Zhang Y, Liu S et al (2020) Alleviation of copper toxicity in Daphnia magna by hydrogen nanobubble water. J Hazard Mater 389:122155. https://doi.org/10.1016/j.jhazmat.2020.122155
Gao F, Li J, Zhang J et al (2022) Genome-wide identification of the ZIP gene family in lettuce (Lactuca sativa L.) and expression analysis under different element stress. PLoS ONE 17:e0274319. https://doi.org/10.1371/journal.pone.0274319
Guan Q, Ding XW, Jiang R et al (2019) Effects of hydrogen-rich water on the nutrient composition and antioxidative characteristics of sprouted black barley. Food Chem 299:125095. https://doi.org/10.1016/j.foodchem.2019.125095
Hanson P, Yang R-y, Chang L-c et al (2009) Contents of carotenoids, ascorbic acid, minerals and total glucosinolates in leafy brassica pakchoi (Brassica rapa L. chinensis) as affected by season and variety. J Sci Food Agr 89:906–914. https://doi.org/10.1002/jsfa.3533
Hsu J, Arcot J, Lee NA (2009) Nitrate and nitrite quantification from cured meat and vegetables and their estimated dietary intake in Australians. Food Chem 115:334–339. https://doi.org/10.1016/j.foodchem.2008.11.081
Hu HL, Li PX, Shen WB (2021) Preharvest application of hydrogen-rich water not only affects daylily bud yield but also contributes to the alleviation of bud browning. Sci Hortic 287:110267. https://doi.org/10.1016/j.scienta.2021.110267
Huang KL, Wang H, Wei YL et al (2019) The high-affinity transporter BnPHT1;4 is involved in phosphorus acquisition and mobilization for facilitating seed germination and early seedling growth of Brassica napus. BMC Plant Biol 19:1–13. https://doi.org/10.1186/s12870-019-1765-3
Iammarino M, Di Taranto A, Cristino M (2014) Monitoring of nitrites and nitrates levels in leafy vegetables (spinach and lettuce): a contribution to risk assessment. J Sci Food Agric 94:773–778. https://doi.org/10.1002/jsfa.6439
Jia Z, Tang M, Wu J (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559. https://doi.org/10.1016/S0308-8146(98)00102-2
Jiang K, Kuang Y, Feng LY et al (2021) Molecular hydrogen maintains the storage quality of Chinese chive through improving antioxidant capacity. Plants 10:1095. https://doi.org/10.3390/plants10061095
Jin QJ, Zhu KK, Cui WT et al (2012) Hydrogen gas acts as a novel bioactive molecule in enhancing plant tolerance to paraquat-induced oxidative stress via the modulation of heme oxygenase-1 signalling system. Plant Cell Environ 36:956–969. https://doi.org/10.1111/pce.12029
Jin ZW, Liu ZY, Chen GM et al (2023) Molecular hydrogen-based irrigation extends strawberry shelf life by improving the synthesis of cell wall components in fruit. Postharvest Biol Technol 206:112551. https://doi.org/10.1016/j.postharvbio.2023.112551
Kang CH, Yoon EK, Muthusamy M et al (2020) Blue LED light irradiation enhances L-ascorbic acid content while reducing reactive oxygen species accumulation in Chinese cabbage seedlings. Sci Hortic 261:108924. https://doi.org/10.1016/j.scienta.2019.108924
Kovač A, Paranos M, Marciuš D (2021) Hydrogen in energy transition: a review. Int J Hydrog Energy 46:10016–10035. https://doi.org/10.1016/j.ijhydene.2020.11.256
Kyriacou MC, Rouphael Y (2018) Towards a new definition of quality for fresh fruits and vegetables. Sci Hortic 234:463–469. https://doi.org/10.1016/j.scienta.2017.09.046
Lairon D (2010) Nutritional quality and safety of organic food: a review. Agron Sustain Dev 30:33–41. https://doi.org/10.1051/agro/2009019
Li Y, Wang XH, Chen ZW et al (2016) Homologous cloning and expression analysis of ascorbic acid biosynthesis gene BcGME under stress from non-heading Chinese cabbage [in Chinese]. J Nanjing Agric Univ 39:205–212
Li LN, Wang J, Jiang K et al (2022) Preharvest application of hydrogen nanobubble water enhances strawberry flavor and consumer preferences. Food Chem 377:131953. https://doi.org/10.1016/j.foodchem.2021.131953
Liu LX, Sun Y, Laura T et al (2009) Determination of polyphenolic content and antioxidant activity of kudingcha made from Ilex kudingcha C.J. Tseng Food Chem 112:35–41. https://doi.org/10.1016/j.foodchem.2008.05.038
Liu FJ, Wang YQ, Zhang GH et al (2022) Molecular hydrogen positively influences lateral root formation by regulating hydrogen peroxide signaling. Plant Sci 325:111500. https://doi.org/10.1016/j.plantsci.2022.111500
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative pcr and the 2−∆∆CT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Luo JK, Sun SB, Jia LJ et al (2006) The mechanism of nitrate accumulation in pakchoi [Brassica campestris L. ssp. Chinensis (L.)]. Plant Soil 282:291–300. https://doi.org/10.1007/s11104-005-6094-7
Martínez S, Armesto J, Gómez-Limia L et al (2020) Impact of processing and storage on the nutritional and sensory properties and bioactive components of Brassica spp. A Review Food Chem 313:126065. https://doi.org/10.1016/j.foodchem.2019.126065
Mattosinhos PDS, Sarandy MM, Novaes RD et al (2022) Anti-inflammatory, antioxidant, and skin regenerative potential of secondary metabolites from plants of the Brassicaceae family: a systematic review of in vitro and in vivo preclinical evidence (biological activities Brassicaceae skin diseases). Antioxidants 11:1346. https://doi.org/10.3390/antiox11071346
Maynard DN, Barker AV, Minotti PL et al (1976) Nitrate accumulation in vegetables. Adv Agron 28:71–118. https://doi.org/10.1016/S0065-2113(08)60553-2
Mitra S, Emran TB, Chandran D et al (2022) Cruciferous vegetables as a treasure of functional foods bioactive compounds: targeting p53 family in gastrointestinal tract and associated cancers. Front Nutr 9:951935. https://doi.org/10.3389/fnut.2022.951935
Ohsawa I, Ishikawa M, Takahashi K et al (2007) Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med 13:688–694. https://doi.org/10.1038/nm1577
Prior RL, Fan E, Ji HP et al (2010) Multi-laboratory validation of a standard method for quantifying proanthocyanidins in cranberry powders. J Sci Food Agric 90:1473–1478. https://doi.org/10.1002/jsfa.3966
Ren J, Chen ZW, Duan WK et al (2013) Comparison of ascorbic acid biosynthesis in different tissues of three non-heading Chinese cabbage cultivars. Plant Physiol Bioch 73:229–236. https://doi.org/10.1016/j.plaphy.2013.10.005
Renwick GM, Giumarro C, Siegel SM (1964) Hydrogen metabolism in higher plants. Plant Physiol 39:303–306. https://doi.org/10.1104/pp.39.3.303
Russell G, Zulfiqar F, Hancock JT (2020) Hydrogenases and the role of molecular hydrogen in plants. Plants 9:1136. https://doi.org/10.3390/plants9091136
Shao YD, Lin F, Wang YQ et al (2023) Molecular hydrogen confers resistance to rice stripe virus. Microbiol Spectr 11:e04417-e4422. https://doi.org/10.1128/spectrum.04417-22
Shi JY, Xiao YH, Jia CL et al (2023) Physiological and biochemical changes during fruit maturation and ripening in highbush blueberry (Vaccinium corymbosum L.). Food Chem 410:135299. https://doi.org/10.1016/j.foodchem.2022.135299
Song YQ, Zhang J, Zhang JB et al (2022) Effect of hydrogen-rich water treatment on the yield and quality of vegetables [in Chinese]. Mod Agric Sci Technol 8:49–54. https://doi.org/10.3969/j.issn.1007-5739.2022.08.017
Stratil P, Klejdus B, Kubáň V (2006) Determination of total content of phenolic compounds and their antioxidant activity in vegetables evaluation of spectrophotometric methods. Agric Food Chem 54:607–616. https://doi.org/10.1021/jf052334j
Su NN, Wu Q, Liu YY et al (2014) Hydrogen-rich water reestablishes ROS homeostasis but exerts differential effects on anthocyanin synthesis in two varieties of radish sprouts under UV-A irradiation. J Agric Food Chem 62:6454–6462. https://doi.org/10.1021/jf5019593
Su JC, Zhang YH, Nie Y et al (2018) Hydrogen-induced osmotic tolerance is associated with nitric oxide-mediated proline accumulation and reestablishment of redox balance in alfalfa seedlings. Environ Exp Bot 147:249–260. https://doi.org/10.1016/j.envexpbot.2017.12.022
Temesgen T, Bui TT, Han M et al (2017) Micro and nanobubble technologies as a new horizon for water-treatment techniques: a review. Adv Colloid Interfac 246:40–51. https://doi.org/10.1016/j.cis.2017.06.011
Utsunomiya Y, Samejima C, Takayanagi Y et al (2011) Suppression of the rice heterotrimeric G protein β-subunit gene, RGB1, causes dwarfism and browning of internodes and lamina joint regions. Plant J 67:907–916. https://doi.org/10.1111/j.1365-313X.2011.04643.x
Wan YY, Wang Z, Xia JC et al (2020) Genome-wide analysis of phosphorus transporter genes in Brassica and their roles in heavy metal stress tolerance. Int J Mol Sci 21:2209. https://doi.org/10.3390/ijms21062209
Wang YQ, Liu YH, Wang S et al (2020) Hydrogen agronomy: research progress and prospects. J Zhejiang Univ Sci B 21:841–855. https://doi.org/10.1631/jzus.B2000386
Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369. https://doi.org/10.1038/30728
Wu Q, Su NN, Cai JT et al (2015) Hydrogen-rich water enhances cadmium tolerance in Chinese cabbage by reducing cadmium uptake and increasing antioxidant capacities. J Plant Physiol 175:174–182. https://doi.org/10.1016/j.jplph.2014.09.017
Xia D, Zhou H, Liu RJ et al (2018) GL3.3, a novel QTL encoding a GSK3/SHAGGY-like kinase, a novel QTL encoding a Gsk3/Shaggy-like kinase, epistatically interacts with GS3 to produce extra-long grains in rice. Mol Plant 11:754–756. https://doi.org/10.1016/j.molp.2018.03.006
Xie YJ, Mao Y, Lai DW et al (2012) H2 enhances Arabidopsis salt tolerance by manipulating ZAT10/12-mediated antioxidant defence and controlling sodium exclusion. PLoS ONE 7:e49800. https://doi.org/10.1371/journal.pone.0049800
Xie YJ, Mao Y, Zhang W et al (2014) Reactive oxygen species-dependent nitric oxide production contributes to hydrogen-promoted stomatal closure in Arabidopsis. Plant Physiol 165:759–773. https://doi.org/10.1104/pp.114.237925
Xie YJ, Zhang W, Duan XL et al (2015) Hydrogen-rich water-alleviated ultraviolet-B-triggered oxidative damage is partially associated with the manipulation of the metabolism of (iso)flavonoids and antioxidant defence in Medicago sativa. Funct Plant Biol 42:1141–1157. https://doi.org/10.1071/FP15204
Xu XY, Yang ZP, Sun XL et al (2014) Selection of reference genes for quantitative real-time PCR during flower bud development in CMS7311 of heading Chinese cabbage (Brassica rapa L. ssp. pekinensis). Acta Physiol Plant 36:809–814. https://doi.org/10.1007/s11738-013-1437-0
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514. https://doi.org/10.1042/bj0570508
Yuan JP, Yu ZH, Lin TT et al (2020) BcERF070, a novel ERF (ethylene-response factor) transcription factor from non-heading Chinese cabbage, affects the accumulation of ascorbic acid by regulating ascorbic acid-related genes. Mol Breed 40:1–18. https://doi.org/10.1007/s11032-019-1065-5
Yuan JP, Li DH, Shen CW et al (2022) Transcriptome analysis revealed the molecular response mechanism of non-heading Chinese cabbage to iron deficiency stress. Front Plant Sci 13:848424. https://doi.org/10.3389/fpls.2022.848424
Zhang XY, Wei JY, Huang YF et al (2018) Increased cytosolic calcium contributes to hydrogen-rich water-promoted anthocyanin biosynthesis under UV-A irradiation in radish sprouts hypocotyls. Front Plant Sci 9:1020. https://doi.org/10.3389/fpls.2018.01020
Zhang YH, Zhao G, Cheng PF et al (2019) Nitrite accumulation during storage of tomato fruit as prevented by hydrogen gas. Int J Food Prop 22:1425–1438. https://doi.org/10.1080/10942912.2019.1651737
Zhang Y, Fan WH, Li XM et al (2022) Enhanced removal of free radicals by aqueous hydrogen nanobubbles and their role in oxidative stress. Environ Sci Technol 56:15096–15107. https://doi.org/10.1021/acs.est.2c03707
Acknowledgements
This work was financially support by the Funding from Air Liquide (China) R&D Co., Ltd., and Shanghai Key Laboratory of Hydrogen Science, Center of Hydrogen Science, Shanghai Jiao Tong University, China.
Author information
Authors and Affiliations
Contributions
ZL: Methodology, Investigation, Writing—review & editing. GC: Methodology, Review & editing. EY: Methodology, Review & editing. LL: Writing—review & editing. YZ: Resources, Review & editing, Validation. XC: Resources, Review & editing, Validation. DP: Review & editing. GX: Review & editing. WS: Conceptualization, Writing—review & editing, Supervision, Funding acquisition.
Corresponding author
Ethics declarations
Conflict of interest
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. Yan Zeng, Xu Cheng, and Didier Pathier are employees and hold ownership interest (including patents) in Air Liquide (China) R&D Co., Ltd.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Liu, Z., Chen, G., Yang, E. et al. Hydrogen-based irrigation increases yield and improves quality of Chinese cabbage by enhancing nutrient composition and antioxidant capabilities. Hortic. Environ. Biotechnol. (2024). https://doi.org/10.1007/s13580-023-00591-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13580-023-00591-2