A static magnetic field improves salt tolerance for poplar cuttings by regulating root reactive oxygen species homeostasis

Jihuai Hu , Wenhao Han , Haojie Zhang , Nianzhao Wang , Guanqing Wu , Qiliang Zhu , Fengyun Ma , Huimei Tian , Yanping Wang

Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1)

PDF
Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) DOI: 10.1007/s11676-025-01859-2
Original Paper

A static magnetic field improves salt tolerance for poplar cuttings by regulating root reactive oxygen species homeostasis

Author information +
History +
PDF

Abstract

A geomagnetic field is a significant factor during the growth and development of trees. Changes in the magnetic field (MF) will result in reactions at the biochemical, molecular, cellular and gene levels. However, it is not clear how a magnetic field affects metabolism and homeostasis under stressful conditions such as salinity. In this study, a novel method was developed of a static magnetic field (SMF) to investigate magnetobiological changes in trees. The results show that pre-treatment of poplar (Populus ×  euramericana ‘Neva’) cuttings with a static magnetic field significantly mitigated the negative effects of salinity stress on their growth and physiological activities. Biochemical assays revealed that several chemical messengers, including hydrogen peroxide (H2O2) and O2•−, were significantly improved in roots treated with salt, implying an increase reactive oxygen species. A static magnetic field also significantly increased proline concentrations, soluble protein contents, and CAT and SOD activities. Electrophysiological experiments further revealed that pre-treatment with a static magnetic field remarkably decreased salt-induced Na+ influx and H+ efflux which control plant salt tolerance. In pharmacological experiments, because the Na+/H+ correlation was closely related to the SMF-activated plasma membrane and Na+ antiporter activity alleviated the massive accumulation of salt-induced reactive oxygen species (ROS) within the roots. In addition, a static magnetic field dramatically increased the transcriptional activity of stress-responsive genes, including PtrRBOHD and PtrHA5. Together, these results indicate that SMF reduced Na+ influx by activating Na+/H+ antiporters and plasma membrane H+-ATPase to effectively maintain homeostasis by regulating the reactive oxygen species system and cytoplasmic osmotic potential. Ultimately, these static magnetic field methods improved salt tolerance in poplar cuttings, and, for future research, similar methods could be applied to other plants.

Keywords

Poplar / Salt tolerance / Static magnetic field / Plasma membrane Na+ transporters / Reactive oxygen species (ROS) homeostasis

Cite this article

Download citation ▾
Jihuai Hu, Wenhao Han, Haojie Zhang, Nianzhao Wang, Guanqing Wu, Qiliang Zhu, Fengyun Ma, Huimei Tian, Yanping Wang. A static magnetic field improves salt tolerance for poplar cuttings by regulating root reactive oxygen species homeostasis. Journal of Forestry Research, 2025, 36(1): DOI:10.1007/s11676-025-01859-2

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

AbdelazizME, AbdelsattarM, AbdeldaymEA, AtiaMAM, MahmoudAWM, SaadMM, HirtH. Piriformospora indica alters Na+/K+ homeostasis, antioxidant enzymes and LeNHX1 expression of greenhouse tomato grown under salt stress. Sci Hortic, 2019, 256 108532

[2]

AfzalI, SaleemS, SkalickyM, JavedT, BakhtavarMA, HaqZU, KamranM, ShahidM, Sohail SaddiqM, AfzalA, ShafqatN, DessokyES, GuptaA, Korczyk-SzaboJ, BresticM, SabaghAEL. Magnetic field treatments improves sunflower yield by inducing physiological and biochemical modulations in seeds. Molecules, 2021, 26(7): 2022

[3]

AgliassaC, MaffeiME. Reduction of geomagnetic field (GMF) to near null magnetic field (NNMF) affects some Arabidopsis thaliana clock genes amplitude in a light independent manner. J Plant Physiol, 2019, 232: 23-26

[4]

BajagićM, ĐukićV, MamlićZM, SekulićJ, CvijanovićV, ĐurićN, CvijanovićG. Effect of pulsed electromagnetic field on yield of grain, yield of protein and oil of soybean. Plant Soil Environ, 2023, 69(12): 577-585

[5]

BekhiteMM, FigullaHR, SauerH, WartenbergM. Static magnetic fields increase cardiomyocyte differentiation of Flk-1+ cells derived from mouse embryonic stem cells via Ca2+ influx and ROS production. Int J Cardiol, 2013, 167(3): 798-808

[6]

Ben RejebK, Lefebvre-De VosD, Le DisquetI, LeprinceAS, BordenaveM, MaldineyR, JdeyA, AbdellyC, SavouréA. Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana. New Phytol, 2015, 208(4): 1138-1148

[7]

BoseJ, Rodrigo-MorenoA, ShabalaS. ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot, 2014, 65(5): 1241-1257

[8]

CalabròE, CondelloS, CurròM, FerlazzoN, CaccamoD, MagazùS, IentileR. Effects of low intensity static magnetic field on FTIR spectra and ROS production in SH-SY5Y neuronal-like cells. Bioelectromagnetics, 2013, 34(8): 618-629

[9]

ChenQH, YangGW. Signal function studies of ROS, especially RBOH-dependent ROS, in plant growth, development and environmental stress. J Plant Growth Regul, 2020, 39(1): 157-171

[10]

ChenZ, LinS, LiJ, ChenT, QuanG, YangT, ZhangZ. Theanine improves salt stress tolerance via modulating redox homeostasis in tea plants (Camellia sinensis L.). Front Plant Sci, 2021, 12: 770398

[11]

ClaussenW. Proline as a measure of stress in tomato plants. Plant Sci, 2005, 168(1): 241-248

[12]

ConsentinoL, LambertS, MartinoC, JourdanN, BouchetPE, WitczakJ, CastelloP, El-EsawiM, CorbineauF, d’HarlingueA, AhmadM. Blue-light dependent reactive oxygen species formation by Arabidopsis cryptochrome may define a novel evolutionarily conserved signaling mechanism. New Phytol, 2015, 206(4): 1450-1462

[13]

da SilvaJAT, DobránszkiJ. How do magnetic fields affect plants in vitro?. In Vitro Cell Dev Biol Plant, 2015, 51(3): 233-240

[14]

De NicolaM, CordiscoS, CerellaC, AlbertiniMC, D’AlessioM, AccorsiA, BergamaschiA, MagriniA, GhibelliL. Magnetic fields protect from apoptosis via redox alteration. Ann N Y Acad Sci, 2006, 1090: 59-68

[15]

DemidchikV, MaathuisFJM. Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol, 2007, 175(3): 387-404

[16]

DemidchikV, ShabalaS, IsayenkovS, CuinTA, PottosinI. Calcium transport across plant membranes: mechanisms and functions. New Phytol, 2018, 220(1): 49-69

[17]

DhawiF, Al-KhayriJM, HassanE. Static magnetic field influence on elements composition in date palm (Phoenix dactylifera L). Res J Agric Biol Sci, 2009, 5(2): 161-166

[18]

DodsonCA, HorePJ, WallaceMI. A radical sense of direction: signalling and mechanism in cryptochrome magnetoreception. Trends Biochem Sci, 2013, 38(9): 435-446

[19]

ElhindiKM, AlmanaFA, Al-YafrsiMA. Role of humic acid on inducing salt tolerance of ivy Geranium (Pelargonium peltatum L) plants. Horticulturae, 2023, 9(9): 1012

[20]

EmreM, CetinerS, ZencirS, UnlukurtI, KahramanI, TopcuZ. Oxidative stress and apoptosis in relation to exposure to magnetic field. Cell Biochem Biophys, 2011, 59(2): 71-77

[21]

FoyerCH, NoctorG. Stress-triggered redox signalling: what’s in pROSpect?. Plant Cell Environ, 2016, 39(5): 951-964

[22]

GongZZ, XiongLM, ShiHZ, YangSH, Herrera-EstrellaLR, XuGH, ChaoDY, LiJR, WangPY, QinF, LiJ, DingYL, ShiYT, WangY, YangYQ, GuoY, ZhuJK. Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci, 2020, 63(5): 635-674

[23]

GuoX, AhmadN, ZhaoSZ, ZhaoCZ, ZhongW, WangXJ, LiGH. Effect of salt stress on growth and physiological properties of Asparagus seedlings. Plants, 2022, 11(21): 2836

[24]

HaghighatN, AbdolmalekiP, GhanatiF, BehmaneshM, PayezA. Modification of catalase and MAPK in Vicia faba cultivated in soil with high natural radioactivity and treated with a static magnetic field. J Plant Physiol, 2014, 171(5): 99-103

[25]

HasanuzzamanM, RaihanMRH, MasudAAC, RahmanK, NowrozF, RahmanM, NaharK, FujitaM. Regulation of reactive oxygen species and antioxidant defense in plants under salinity. Int J Mol Sci, 2021, 22(17): 9326

[26]

HorePJ. Are biochemical reactions affected by weak magnetic fields?. Proc Natl Acad Sci USA, 2012, 109(5): 1357-1358

[27]

HuJH, ZhangHJ, HanWH, WangNZ, MaSQ, MaFY, TianHM, WangYP. Physiological responses revealed static magnetic fields potentially improving the tolerance of poplar seedlings to salt stress. Forests, 2024, 15(1): 138

[28]

IkeyaN, WoodwardJR. Cellular autofluorescence is magnetic field sensitive. Proc Natl Acad Sci USA, 2021, 118(3): e2018043118

[29]

IslamM, MaffeiME, ViganiG. The geomagnetic field is a contributing factor for an efficient iron uptake in Arabidopsis thaliana. Front Plant Sci, 2020, 11: 325

[30]

JiangMY, ZhangJH. Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot, 2002, 53(379): 2401-2410

[31]

JiangXC, YangYC, FengSY, HuYW, CaoM, LuoJ. Reactive effects of pre-sowing magnetic field exposure on morphological characteristics and antioxidant ability of Brassica juncea in phytoextraction. Chemosphere, 2022, 303(Pt 1): 135046

[32]

KattnigDR. Radical-pair-based magnetoreception amplified by radical scavenging: resilience to spin relaxation. J Phys Chem B, 2017, 121(44): 10215-10227

[33]

LiJ, BaoSQ, ZhangYH, MaXJ, Mishra-KnyrimM, SunJ, SaG, ShenX, PolleA, ChenSL. Paxillus involutus strains MAJ and NAU mediate K(+)/Na(+) homeostasis in ectomycorrhizal Populus × canescens under sodium chloride stress. Plant Physiol, 2012, 159(4): 1771-1786

[34]

LiWQ, ZhengWJ, PengY, ShaoY, LiuCT, LiJ, HuYY, ZhaoBR, MaoBG. OsPMS1 mutation enhances salt tolerance by suppressing ROS accumulation, maintaining Na+/K+ homeostasis, and promoting ABA biosynthesis. Genes, 2023, 14(8): 1621

[35]

Lopresto V, Merla C, Pinto R, Benvenuto E (2015) High-intensity static magnetic field exposure devices for in vitro experiments on biopharmaceutical plant factories in aerospace environments. In: 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC). Milan, Italy. IEEE

[36]

LoretoF, VelikovaV. Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol, 2001, 127(4): 1781-1787

[37]

LuoD, SongFH, LuMY, ShiYJ, MaQH. Salt-stress-induced ion transport contributes to K+/Na+ homeostasis in roots of Ping’ou hybrid hazelnut. Forests, 2023, 14(8): 1651

[38]

MaedaK, RobinsonAJ, HenbestKB, HogbenHJ, BiskupT, AhmadM, SchleicherE, WeberS, TimmelCR, HorePJ. Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor. Proc Natl Acad Sci USA, 2012, 109(13): 4774-4779

[39]

MaffeiME. Magnetic field effects on plant growth, development, and evolution. Front Plant Sci, 2014, 5: 445

[40]

McGinleyJVM, RisticM, YoungIR. A permanent MRI magnet for magic angle imaging having its field parallel to the poles. J Magn Reson, 2016, 271: 60-67

[41]

MeiXD, DaiT, ShenYB. Adaptive strategy of Nitraria sibirica to transient salt, alkali and osmotic stresses via the alteration of Na+/K+ fluxes around root tips. J Forestry Res, 2023, 34(2): 425-432

[42]

MittlerR, ZandalinasSI, FichmanY, Van BreusegemF. Reactive oxygen species signalling in plant stress responses. Nat Rev Mol Cell Biol, 2022, 23(10): 663-679

[43]

MondalP, Huix-RotllantM. Theoretical insights into the formation and stability of radical oxygen species in cryptochromes. Phys Chem Chem Phys, 2019, 21(17): 8874-8882

[44]

NarayanaR, FliegmannJ, PaponovI, MaffeiME. Reduction of geomagnetic field (GMF) to near null magnetic field (NNMF) affects Arabidopsis thaliana root mineral nutrition. Life Sci Space Res, 2018, 19: 43-50

[45]

NyakaneNE, SedibeMM, MarkusE. Growth Response of Rose Geranium (Pelargonium graveolens L.) to Calcium:Magnesium Ratio, Magnetic Field, and Mycorrhizae. HortScience, 2019, 54(10): 1762-1768

[46]

OcchipintiA, De SantisA, MaffeiME. Magnetoreception: an unavoidable step for plant evolution?. Trends Plant Sci, 2014, 19(1): 1-4

[47]

OgunsijiE, UmebeseC, StabentheinerE, IwualaE, OdjegbaV, OluwajobiA. Salicylic acid enhances growth, photosynthetic performance and antioxidant defense activity under salt stress in two mungbean [Vigna radiata (L.) R. Wilczek] variety. Plant Signal Behav, 2023, 18(1): 2217605

[48]

PlayerTC, HorePJ. Viability of superoxide-containing radical pairs as magnetoreceptors. J Chem Phys, 2019, 151(22): 225101

[49]

RadhakrishnanR. Magnetic field regulates plant functions, growth and enhances tolerance against environmental stresses. Physiol Mol Biol Plants, 2019, 25(5): 1107-1119

[50]

RadhakrishnanR, LeelapriyaT, KumariBDR. Effects of pulsed magnetic field treatment of soybean seeds on calli growth, cell damage, and biochemical changes under salt stress. Bioelectromagnetics, 2012, 33(8): 670-681

[51]

RehmanM, MaqboolZ, PengDX, LiuLJ. Morpho-physiological traits, antioxidant capacity and phytoextraction of copper by ramie (Boehmeria nivea L) grown as fodder in copper-contaminated soil. Environ Sci Pollut Res Int, 2019, 26(6): 5851-5861

[52]

ReinaFG, PascualLA. Influence of a stationary magnetic field on water relations in lettuce seeds Part i: Theoretical Considerations. Bioelectromagnetics, 2001, 22(8): 589-595

[53]

SaletnikB, SaletnikA, SłyszE, ZagułaG, BajcarM, Puchalska-SarnaA, PuchalskiC. The static magnetic field regulates the structure, biochemical activity, and gene expression of plants. Molecules, 2022, 27(18): 5823

[54]

SarrafM, DeamiciKM, TaimouryaH, IslamM, KatariaS, RaipuriaRK, AbdiG, BresticM. Effect of magnetopriming on photosynthetic performance of plants. Int J Mol Sci, 2021, 22(17): 9353

[55]

SewelamN, KazanK, SchenkPM. Global plant stress signaling: reactive oxygen species at the cross-road. Front Plant Sci, 2016, 7: 187

[56]

ShabrangyA, GhatakA, ZhangS, PrillerA, ChaturvediP, WeckwerthW. Magnetic field induced changes in the shoot and root proteome of barley (Hordeum vulgare L). Front Plant Sci, 2021, 12: 622795

[57]

ShineMB, GuruprasadKN, AnandA. Effect of stationary magnetic field strengths of 150 and 200 mT on reactive oxygen species production in soybean. Bioelectromagnetics, 2012, 33(5): 428-437

[58]

SiesH. Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: Oxidative eustress. Redox Biol, 2017, 11: 613-619

[59]

SiesH, JonesDP. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat Rev Mol Cell Biol, 2020, 21(7): 363-383

[60]

SiesH, BerndtC, JonesDP. Oxidative stress. Annu Rev Biochem, 2017, 86: 715-748

[61]

Solov’yovIA, ChandlerDE, SchultenK. Magnetic field effects in Arabidopsis thaliana cryptochrome-1. Biophys J, 2007, 92(8): 2711-2726

[62]

SunJ, ChenSL, DaiSX, WangRG, LiNY, ShenX, ZhouXY, LuCF, ZhengXJ, HuZM, ZhangZK, SongJ, XuY. NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species. Plant Physiol, 2009, 149(2): 1141-1153

[63]

SunJ, WangMJ, DingMQ, DengSR, LiuMQ, LuCF, ZhouXY, ShenX, ZhengXJ, ZhangZK, SongJ, HuZM, XuY, ChenSL. H2O2 and cytosolic Ca2+ signals triggered by the PM H-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. Plant Cell Environ, 2010, 33(6): 943-958

[64]

SuzukiN, MillerG, MoralesJ, ShulaevV, TorresMA, MittlerR. Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol, 2011, 14(6): 691-699

[65]

TerziA, SuterDM. The role of NADPH oxidases in neuronal development. Free Radic Biol Med, 2020, 154: 33-47

[66]

WangHZ, ZhangX. Magnetic fields and reactive oxygen species. Int J Mol Sci, 2017, 18(10): 2175

[67]

WangRG, ChenSL, ZhouXY, ShenX, DengL, ZhuHJ, ShaoJ, ShiY, DaiSX, FritzE, HüttermannA, PolleA. Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress. Tree Physiol, 2008, 28(6): 947-957

[68]

WaszczakC, CarmodyM, KangasjärviJ. Reactive oxygen species in plant signaling. Annu Rev Plant Biol, 2018, 69: 209-236

[69]

XuJJ, JarochaLE, ZollitschT, KonowalczykM, HenbestKB, RichertS, GolesworthyMJ, SchmidtJ, DéjeanV, SowoodDJC, BassettoM, LuoJT, WaltonJR, FlemingJ, WeiYJ, PitcherTL, MoiseG, HerrmannM, YinH, WuHJ, BartölkeR, KäsehagenSJ, HorstS, DautajG, MurtonPDF, GehrckensAS, ChelliahY, TakahashiJS, KochKW, WeberS, Solov’yovIA, XieC, MacKenzieSR, TimmelCR, MouritsenH, HorePJ. Magnetic sensitivity of cryptochrome 4 from a migratory songbird. Nature, 2021, 594(7864): 535-540

[70]

YangYQ, GuoY. Unraveling salt stress signaling in plants. J Integr Plant Biol, 2018, 60(9): 796-804

[71]

YuYF, ZhangM, FengJY, SunSJ, ZhouP, YangJD. Physiological analysis reveals relatively higher salt tolerance in roots of Ilex integra than in those of Ilex purpurea. J Forestry Res, 2022, 33: 1187-1196

[72]

Zadeh-HaghighiH, SimonC. Magnetic field effects in biology from the perspective of the radical pair mechanism. J R Soc Interface, 2022, 19(193): 20220325

[73]

ZhangHL, ZhangYN, DengC, DengSR, LiNF, ZhaoCJ, ZhaoR, LiangS, ChenSL. The Arabidopsis Ca2+-dependent protein kinase CPK12 is involved in plant response to salt stress. Int J Mol Sci, 2018, 19(12): 4062

[74]

ZhangHL, DengC, WuX, YaoJ, ZhangYL, ZhangYN, DengSR, ZhaoN, ZhaoR, ZhouXY, LuCF, LinSZ, ChenSL. Populus euphratica remorin 65 activates plasma membrane H+-ATPases to mediate salt tolerance. Tree Physiol, 2020, 40(6): 731-745

[75]

ZhangJS, WangYQ, SongJN, XuJP, YangHB. Effect of aspartic acid on physiological characteristics and gene expression of salt exclusion in Tartary buckwheat under salt stress. J Plant Biochem Biotechnol, 2020, 29(1): 94-101

[76]

ZhangHM, ZhuJH, GongZZ, ZhuJK. Abiotic stress responses in plants. Nat Rev Genet, 2022, 23(2): 104-119

[77]

ZhaoN, WangSJ, MaXJ, ZhuHP, SaG, SunJ, LiNF, ZhaoCJ, ZhaoR, ChenSL. Extracellular ATP mediates cellular K+/Na+ homeostasis in two contrasting poplar species under NaCl stress. Trees, 2016, 30(3): 825-837

[78]

ZhuJK. Plant salt tolerance. Trends Plant Sci, 2001, 6(2): 66-71

RIGHTS & PERMISSIONS

Northeast Forestry University

AI Summary AI Mindmap
PDF

226

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/