Hydrogen-rich water promotes elongation of hypocotyls and roots in plants through mediating the level of endogenous gibberellin and auxin
Qi Wu A B , Nana Su B , Xin Huang A , Xiaoping Ling A , Min Yu A , Jin Cui B D and Sergey Shabala
A C D
+ Author Affiliations
- Author Affiliations
A International Research Centre for Environmental Membrane Biology, Foshan University, Foshan 528000, China.
B College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China.
C Tasmanian Institute of Agriculture, College of Science and Engineering, University of Tasmania, Hobart, Tas. 7001, Australia.
D Corresponding authors. Email: cuijin@njau.edu.cn; sergey.shabala@utas.edu.au
Functional Plant Biology 47(9) 771-778 https://doi.org/10.1071/FP19107
Submitted: 10 September 2019 Accepted: 1 April 2020 Published: 11 June 2020
Abstract
The aim of this study was to investigate effects of the hydrogen-rich water (HRW) on the vegetable growth, and explore the possibility of applying HRW for protected cultivation of vegetables. Results showed that compared with control, HRW treatment significantly promoted fresh weight, hypocotyl length and root length of mung bean seedlings. The strongest stimulation was observed for 480 μM H2 (60% of saturated HRW concentration) treatment. This concentration was used in the following experiments. The enhanced cell elongation was correlated with the changes in the level of endogenous phytohormones. In the dark-grown hypocotyls and roots of mung bean seedlings, HRW significantly increased the content of IAA and GA3. Addition of GA3 enhanced the hypocotyl elongation only. uniconazole, an inhibitor of GA3 biosynthesis, inhibited HRW-induced hypocotyl elongation, but did not affect root elongation. Exogenous application of IAA promoted HRW effects on elongation of both the hypocotyl and the root, while the IAA biosynthesis inhibitor TIBA negated the above affects. The general nature of HRW-induced growth-promoting effects was further confirmed in experiments involving cucumber and radish seedlings. Taken together, HRW treatment promoted growth of seedlings, by stimulating elongation of hypocotyl and root cells, via HRW-induced increase in GA and IAA content in the hypocotyl and the root respectively.
Additional keywords: cell length, hypocotyl elongation, mung bean seedlings, plant hormones, root elongation.
References
Asgher M, Per TS, Masood A, Fatma M, Freschi L, Corpas FJ, Khan NA (2017) Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress. Environmental Science and Pollution Research International 24, 2273–2285.| Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress.Crossref | GoogleScholarGoogle Scholar | 27812964PubMed |
Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annual Review of Genetics 43, 265–285.
| Mechanism of auxin-regulated gene expression in plants.Crossref | GoogleScholarGoogle Scholar | 19686081PubMed |
Chen M, Cui W, Zhu K, Xie Y, Zhang C, Shen W (2014) Hydrogen-rich water alleviates aluminum-induced inhibition of root elongation in alfalfa via decreasing nitric oxide production. Journal of Hazardous Materials 267, 40–47.
| Hydrogen-rich water alleviates aluminum-induced inhibition of root elongation in alfalfa via decreasing nitric oxide production.Crossref | GoogleScholarGoogle Scholar | 24413050PubMed |
Chen Y, Wang M, Hu L, Liao W, Dawuda MM, Li C (2017) Carbon monoxide is involved in hydrogen gas-induced adventitious root development in cucumber under simulated drought stress. Frontiers in Plant Science 8, 128
| Carbon monoxide is involved in hydrogen gas-induced adventitious root development in cucumber under simulated drought stress.Crossref | GoogleScholarGoogle Scholar | 28223992PubMed |
Claeys H, De B, Inze D (2014) Gibberellins and DELLAs: central nodes in growth regulatory networks. Trends in Plant Science 19, 231–239.
| Gibberellins and DELLAs: central nodes in growth regulatory networks.Crossref | GoogleScholarGoogle Scholar | 24182663PubMed |
Davies PJ (2004) ‘Plant hormones-biosynthesis, signal transduction, action!’ (Kluwer Academic Publishers: Dordrecht, Netherlands)
de Wit M, Galvão V, Fankhauser C (2016) Light-mediated hormonal regulation of plant growth and development. Annual Review of Plant Biology 67, 513–537.
| Light-mediated hormonal regulation of plant growth and development.Crossref | GoogleScholarGoogle Scholar | 26905653PubMed |
Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445.
| The F-box protein TIR1 is an auxin receptor.Crossref | GoogleScholarGoogle Scholar | 15917797PubMed |
Dong ZM, Layzell DB (2001) H2 oxidation, O2 uptake and CO2 fixation in hydrogen treated soils. Plant Soil 229, 1–12.
| H2 oxidation, O2 uptake and CO2 fixation in hydrogen treated soils.Crossref | GoogleScholarGoogle Scholar |
Hu H, Li P, Wang Y, Gu R (2014) Hydrogen-rich water delays postharvest ripening and senescence of kiwifruit. Food Chemistry 156, 100–109.
| Hydrogen-rich water delays postharvest ripening and senescence of kiwifruit.Crossref | GoogleScholarGoogle Scholar | 24629944PubMed |
Huang KL, Ma G, Zhang M, Xiong H, Wu H, Zhao C, Liu C, Jia H, Chen L, Kjorven J, Li X, Ren F (2018) The ARF7 and ARF19 transcription factors positivity regulate PHOSPHATE STARVATION RESPONSE1 in Arabidopsis roots. Plant Physiology 178, 413–427.
| The ARF7 and ARF19 transcription factors positivity regulate PHOSPHATE STARVATION RESPONSE1 in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 30026290PubMed |
Ito S, Yamagami D, Umehara M, Hanada A, Yoshida S, Sasaki Y, Yajima S, Kyozuka J, Uequchi-Tanaka M, Matsuoka M, Shirasu K, Yamaquchi S, Asami T (2017) Regulation of strigolactone biosynthesis by gibberellin signaling. Plant Physiology 174, 1250–1259.
| Regulation of strigolactone biosynthesis by gibberellin signaling.Crossref | GoogleScholarGoogle Scholar | 28404726PubMed |
Jin Q, Zhu K, Cui W, Li L, Shen W (2016) Hydrogen-modulated stomatal sensitivity to abscisic acid and drought tolerance via the regulation of apoplastic pH in Medicago sativa. Journal of Plant Growth Regulation 35, 565–573.
| Hydrogen-modulated stomatal sensitivity to abscisic acid and drought tolerance via the regulation of apoplastic pH in Medicago sativa.Crossref | GoogleScholarGoogle Scholar |
Khanna N, Lindblad P (2015) Cyanobacterial hydrogenases and hydrogen metabolism revisited: recent progress and future prospects. International Journal of Molecular Sciences 16, 10537–10561.
| Cyanobacterial hydrogenases and hydrogen metabolism revisited: recent progress and future prospects.Crossref | GoogleScholarGoogle Scholar | 26006225PubMed |
Kurepin LV, Pharis RP (2014) Light signaling and the phytohormonal regulation of shoot growth. Plant Science 229, 280–289.
| Light signaling and the phytohormonal regulation of shoot growth.Crossref | GoogleScholarGoogle Scholar | 25443853PubMed |
Lau OS, Deng XW (2010) Plant hormone signaling lightens up: integrators of light and hormones. Current Opinion in Plant Biology 13, 571–577.
| Plant hormone signaling lightens up: integrators of light and hormones.Crossref | GoogleScholarGoogle Scholar | 20739215PubMed |
Lin Y, Zhang W, Qi F, Cui W, Xie Y, Shen W (2014) Hydrogen-rich water regulates cucumber adventitious root development in a heme oxygenase-1/carbon monoxide-dependent manner. Journal of Plant Physiology 171, 1–8.
| Hydrogen-rich water regulates cucumber adventitious root development in a heme oxygenase-1/carbon monoxide-dependent manner.Crossref | GoogleScholarGoogle Scholar | 24331413PubMed |
Liu H, Li X, Xiao J, Wang S (2012) A convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interaction. Plant Methods 8, 2
| A convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interaction.Crossref | GoogleScholarGoogle Scholar | 22243810PubMed |
Liu F, Li J, Liu Y (2016a) Molecular hydrogen can take part in phytohormone signal pathways in wild rice. Biologia Plantarum 60, 311–319.
| Molecular hydrogen can take part in phytohormone signal pathways in wild rice.Crossref | GoogleScholarGoogle Scholar |
Liu Y, Han S, Ding X, Li X, Zhang L, Li W, Xu H, Li Z, Qi L (2016b) Transcriptome analysis of mRNA and miRNA in somatic embryos of Larix leptolepis subjected to hydrogen treatment. International Journal of Molecular Sciences 17, 1951
| Transcriptome analysis of mRNA and miRNA in somatic embryos of Larix leptolepis subjected to hydrogen treatment.Crossref | GoogleScholarGoogle Scholar |
Nambara E, Akazawa T, Peter M (1991) Effects of the gibberellin biosynthetic inhibitor uniconazol on mutants of Arabidopsis. Plant Physiology 97, 736–738.
| Effects of the gibberellin biosynthetic inhibitor uniconazol on mutants of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 16668460PubMed |
Pan X, Welti R, Wang X (2010) Simultaneous quantification of major phytohormones and related compounds in crude plant extracts by liquid chromatography-electrospray tandem mass spectrometry. Nature Protocols 5, 986–992.
| Simultaneous quantification of major phytohormones and related compounds in crude plant extracts by liquid chromatography-electrospray tandem mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 20448544PubMed |
Renwick GM, Giumarro C, Siegel SM (1964) Hydrogen metabolism in higher plant. Plant Physiology 39, 303–306.
| Hydrogen metabolism in higher plant.Crossref | GoogleScholarGoogle Scholar | 16655917PubMed |
Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459, 1071–1078.
| Recent advances and emerging trends in plant hormone signalling.Crossref | GoogleScholarGoogle Scholar |
Santner A, Calderonvillalobos L, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nature Chemical Biology 5, 301–307.
| Plant hormones are versatile chemical regulators of plant growth.Crossref | GoogleScholarGoogle Scholar | 19377456PubMed |
Su N, Wu Q, Liu Y, Cai J, Shen W, Xia K, Cui J (2014) Hydrogen-rich water reestablishes ROS homeostasis but exerts differential effects on anthocyanin synthesis in two varieties of radish sprouts under UV-A irradiation. Journal of Agricultural and Food Chemistry 62, 6454–6462.
| Hydrogen-rich water reestablishes ROS homeostasis but exerts differential effects on anthocyanin synthesis in two varieties of radish sprouts under UV-A irradiation.Crossref | GoogleScholarGoogle Scholar | 24955879PubMed |
Takatsuka H, Umeda M (2014) Hormonal control of cell division and elongation along differentiation trajectories in roots. Journal of Experimental Botany 65, 2633–2643.
| Hormonal control of cell division and elongation along differentiation trajectories in roots.Crossref | GoogleScholarGoogle Scholar | 24474807PubMed |
Taylor CB (1997) Plant vegetative development: from seed and embryo to shoot and root. The Plant Cell 9, 981–988.
| Plant vegetative development: from seed and embryo to shoot and root.Crossref | GoogleScholarGoogle Scholar | 12237370PubMed |
Torres V, Ballesteros A, Fernández VM (1986) Expression of hydrogenase activity in barley (Hordeum vulgare L.) after anaerobic stress. Archives of Biochemistry and Biophysics 245, 174–178.
| Expression of hydrogenase activity in barley (Hordeum vulgare L.) after anaerobic stress.Crossref | GoogleScholarGoogle Scholar | 3511850PubMed |
Tsukagoshi H (2016) Control of root growth and development by reactive oxygen species. Current Opinion in Plant Biology 29, 57–63.
| Control of root growth and development by reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 26724502PubMed |
Ueguchi-Tanaka M, Hirano K, Hasegawa Y, Kitano H, Matsuoka M (2008) Release of the repressive activity of rice DELLA protein SLR1 by gibberellin does not require SLR1 degradation in the gid2 mutant. The Plant Cell 20, 2437–2446.
| Release of the repressive activity of rice DELLA protein SLR1 by gibberellin does not require SLR1 degradation in the gid2 mutant.Crossref | GoogleScholarGoogle Scholar | 18827181PubMed |
Van de Poel B, Smet D, Van Der Straeten D (2015) Ethylene and hormonal crosstalk in vegetative growth and development. Plant Physiology 169, 61–72.
| Ethylene and hormonal crosstalk in vegetative growth and development.Crossref | GoogleScholarGoogle Scholar | 26232489PubMed |
Vandenbussche F, Verbelen JP, Van Der Straeten D (2005) Of light and length: regulation of hypocotyl growth in Arabidopsis. BioEssays 27, 275–284.
| Of light and length: regulation of hypocotyl growth in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 15714558PubMed |
Verma V, Ravindran P, Kumar P (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biology 16, 86
| Plant hormone-mediated regulation of stress responses.Crossref | GoogleScholarGoogle Scholar | 27079791PubMed |
Wu Q, Su N, Cai J, Shen Z, Cui J (2015) Hydrogen-rich water enhances cadmium tolerance in Chinese cabbage by reducing cadmium uptake and increasing antioxidant capacities. Journal of Plant Physiology 175, 174–182.
| Hydrogen-rich water enhances cadmium tolerance in Chinese cabbage by reducing cadmium uptake and increasing antioxidant capacities.Crossref | GoogleScholarGoogle Scholar | 25543863PubMed |
Xie Y, Mao Y, Lai D, Zhang W, Shen W (2012) H2 enhances Arabidopsis salt tolerance by manipulating ZAT10/12-mediated antioxidant defence and controlling sodium exclusion. PLoS One 7, e49800
| H2 enhances Arabidopsis salt tolerance by manipulating ZAT10/12-mediated antioxidant defence and controlling sodium exclusion.Crossref | GoogleScholarGoogle Scholar | 23300932PubMed |
Xie Y, Mao Y, Zhang W, Lai D, Wang Q, Shen W (2014) Reactive oxygen species-dependent nitric oxide production contributes to hydrogen-promoted stomatal closure in Arabidopsis. Plant Physiology 165, 759–773.
| Reactive oxygen species-dependent nitric oxide production contributes to hydrogen-promoted stomatal closure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24733882PubMed |
Xie Y, Zhang W, Duan X, Dai C, Zhang Y, Cui W, Wang R, Shen W (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. Functional Plant Biology 42, 1141–1157.
| 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.Crossref | GoogleScholarGoogle Scholar | 32480752PubMed |
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annual Review of Plant Biology 59, 225–251.
| Gibberellin metabolism and its regulation.Crossref | GoogleScholarGoogle Scholar | 18173378PubMed |
Zeng J, Zhang M, Sun X (2013) Carbon monoxide is involved in hydrogen gas-induced adventitious root development in cucumber under simulated drought stress. PLoS One 8, e71083
Zeng J, Ye Z, Sun X (2014) Progress in the study of biological effects of hydrogen on higher plants and its promising application in agriculture. Medical Gas Research 4, 15
| Progress in the study of biological effects of hydrogen on higher plants and its promising application in agriculture.Crossref | GoogleScholarGoogle Scholar | 25276344PubMed |
Zheng M, Liu X, Liang S, Fu S, Qi Y, Zhao J, Shao J, An L, Yu F (2016) Chloroplast translation initiation factors regulate leaf variegation and development. Plant Physiology 172, 1117–1130.
| Chloroplast translation initiation factors regulate leaf variegation and development.Crossref | GoogleScholarGoogle Scholar | 27535792PubMed |
Zhu Y, Liao W (2016) A positive role for hydrogen gas in adventitious root development. Plant Signaling & Behavior 11, e1187359
| A positive role for hydrogen gas in adventitious root development.Crossref | GoogleScholarGoogle Scholar |
