Ozone exposure alters nutrients and stoichiometric ratios in different organs of four urban tree species despite limited negative effects on leaf physiology and plant growth and biomass

Kun Zhang , Shenglan Li , Shuangjiang Li , Bo Shang , Costas J. Saitanis , Yansen Xu , Chao Fang , George Papadopoulos , Zhaozhong Feng , Evgenios Agathokleous

Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) : 29

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Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) : 29 DOI: 10.1007/s11676-025-01823-0
Original Paper

Ozone exposure alters nutrients and stoichiometric ratios in different organs of four urban tree species despite limited negative effects on leaf physiology and plant growth and biomass

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Abstract

To better understand the effects of ground-level ozone (O3) on nutrients and stoichiometry in different plant organs, urban tree species Celtis sinensis, Cyclocarya paliurus, Quercus acutissima, and Quercus nuttallii were subjected to a constant exposure to charcoal-filtered air (CF), nonfiltered air (NF), or NF + 40, 60, or 80 nmol O3 mol–1 (NF40, NF60, and NF80) starting early in the summer of the growing season. At the end of summer, net CO2 assimilation rate (A), stomatal conductance (gs), leaf mass per area (LMA), and/or leaf greenness (SPAD) either were not significantly affected by elevated O3 or were even higher in some cases during the summer compared with the CF or NF controls. LMA was significantly lower in autumn only after the highest O3 exposures. Compared to NF, NF40 caused a large increase in gs across species in late summer and more K and Mn in stems. At the end of the growing season, nutrient status and stoichiometric ratios in different organs were variously altered under O3 stress; many changes were large and often species-specific. Across O3 treatments, LMA was primarily associated with C and Mg levels in leaves and Ca levels in leaves and stems. NF40 enriched K, P, Fe, and Mn in stems, relative to NF, and NF60 enhanced Ca in leaves relative to CF and NF40. Moreover, NF resulted in a higher Ca/Mg ratio in leaves of Q. acutissima only, relative to the other O3 regimes. Interestingly, across species, O3 stress led to different nutrient modifications in different organs (stems + branches vs leaves). Thus, ambient and/or elevated O3 exposures can alter the dynamics and distribution of nutrients and disrupt stoichiometry in different organs in a species-specific manner. Changes in stoichiometry reflect an important defense mechanism in plants under O3, and O3 pollution adds more risk to ecological stoichiometries in urban areas.

Keywords

Air pollution / Ground-level ozone / Urban green / Micronutrients / Nutrient cycling

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Kun Zhang, Shenglan Li, Shuangjiang Li, Bo Shang, Costas J. Saitanis, Yansen Xu, Chao Fang, George Papadopoulos, Zhaozhong Feng, Evgenios Agathokleous. Ozone exposure alters nutrients and stoichiometric ratios in different organs of four urban tree species despite limited negative effects on leaf physiology and plant growth and biomass. Journal of Forestry Research, 2025, 36(1): 29 DOI:10.1007/s11676-025-01823-0

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References

[1]

AgathokleousE, SaitanisCJ. Plant susceptibility to ozone: a tower of babel?. Sci Total Environ, 2020, 703 134962

[2]

AgathokleousE, SaitanisCJ, StamatelopoulosD, Mouzaki-PaxinouAC, PaolettiE, ManningWJ. Olive oil for dressing plant leaves so as to avoid O3 injury. Water Air Soil Pollut, 2016, 227(8): 282

[3]

AgathokleousE, KitaoM, ChuQN, SaitanisCJ, PaolettiE, ManningWJ, WatanabeT, KoikeT. Effects of ozone (O3) and ethylenediurea (EDU) on the ecological stoichiometry of a willow grown in a free-air exposure system. Environ Pollut, 2018, 238: 663-676

[4]

AgathokleousE, KitaoM, KoikeT. Ethylenediurea (EDU) effects on hybrid larch saplings exposed to ambient or elevated ozone over three growing seasons. J for Res, 2022, 33(1): 117-135

[5]

AgathokleousE, SaitanisCJ, AgathokleousS, SavvidesC, CalatayudV, SicardP. isoAOT40: an improved ozone exposure index based on the Annual Ozone Spectrum Profile (AO3SP). J for Res, 2022, 33(6): 1949-1955

[6]

AlejandroS, HöllerS, MeierB, PeiterE. Manganese in plants: from acquisition to subcellular allocation. Front Plant Sci, 2020, 11: 300

[7]

AllenAP, GilloolyJF. Towards an integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling. Ecol Lett, 2009, 12(5): 369-384

[8]

BadiaA, VidalV, VenturaS, CurcollR, SeguraR, VillalbaG. Modelling the impacts of emission changes on O3 sensitivity, atmospheric oxidation capacity, and pollution transport over the Catalonia region. Atmos Chem Phys, 2023, 23(18): 10751-10774

[9]

BhattaraiH, TaiAPK, Val MartinM, YungDHY. Impacts of changes in climate, land use, and emissions on global ozone air quality by mid-21st century following selected Shared Socioeconomic Pathways. Sci Total Environ, 2024, 906 167759

[10]

BloomAJ, LancasterKM. Manganese binding to Rubisco could drive a photorespiratory pathway that increases the energy efficiency of photosynthesis. Nat Plants, 2018, 4(7): 414-422

[11]

BoxGEP, CoxDR. An analysis of transformations. J R Stat Soc Ser B Stat Methodol, 1964, 26(2): 211-243

[12]

CalabreseEJ, MattsonMP. How does hormesis impact biology, toxicology, and medicine?. NPJ Aging Mech Dis, 2017, 3: 13

[13]

CaoJX, ShangH, ChenZ, TianY, YuH. Effects of elevated ozone on stoichiometry and nutrient pools of Phoebe bournei (hemsl.) Yang and Phoebe zhennan S lee et F. N. Wei seedlings in subtropical China. Forests, 2016, 7(4): 78

[14]

CarvalhoMEA, CastroPRC, AzevedoRA. Hormesis in plants under Cd exposure: from toxic to beneficial element?. J Hazard Mater, 2020, 384 121434

[15]

ChenZL, JianYQ, WuQ, WuJ, ShengWB, JiangS, ShehlaN, AmanS, WangW. Cyclocarya paliurus (Batalin) Iljinskaja: botany, ethnopharmacology, phytochemistry and pharmacology. J Ethnopharmacol, 2022, 285 114912

[16]

CohenJStatistical power analysis for the behavioral sciences, 2013Routledge

[17]

CostantiniD. Hormesis promotes evolutionary change. Dose Response, 2019, 17(2): 1559325819843376

[18]

CostantiniDCostantiniD, MarascoV. For better or worse: benefits and costs of transgenerational plasticity and the transhormesis hypothesis. Development Strategies and Biodiversity: Darwinian Fitness and Evolution in the Anthropocene, 2022, Cham, Springer International Publishing: 37-49

[19]

CostantiniD, BorremansB. The linear no-threshold model is less realistic than threshold or hormesis-based models: an evolutionary perspective. Chem Biol Interact, 2019, 301: 26-33

[20]

CostantiniD, MetcalfeNB, MonaghanP. Ecological processes in a hormetic framework. Ecol Lett, 2010, 13(11): 1435-1447

[21]

CotrozziL. The effects of tropospheric ozone on oaks: a global meta-analysis. Sci Total Environ, 2021, 756 143795

[22]

ElansaryHO, SzopaA, KubicaP, EkiertH, MattarMA, Al-YafrasiMA, El-AnsaryDO, El-AbedinTKZ, YessoufouK. Polyphenol profile and pharmaceutical potential of Quercus spp. bark extracts. Plants, 2019, 8(11): 486

[23]

ElserJJ, FaganWF, KerkhoffAJ, SwensonNG, EnquistBJ. Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol, 2010, 186(3): 593-608

[24]

EmbersonL. Effects of ozone on agriculture, forests and grasslands. Philos Trans A Math Phys Eng Sci, 2020, 378(2183): 20190327

[25]

ErofeevaEA. Plant hormesis and Shelford’s tolerance law curve. J Forestry Res, 2021, 32(5): 1789-1802

[26]

ErofeevaEA. Environmental hormesis: from cell to ecosystem. Curr Opin Environ Sci Health, 2022, 29 100378

[27]

ErofeevaEA, GelashviliDB, RozenbergGS. The modern concept of hormesis: an overview of the issue and its significance for ecology. Biol Bull Rev, 2023, 13(3): S229-S239

[28]

Esmeijer-LiuAJ, AertsR, KürschnerWM, BobbinkR, LotterAF, VerhoevenJTA. Nitrogen enrichment lowers Betula pendula green and yellow leaf stoichiometry irrespective of effects of elevated carbon dioxide. Plant Soil, 2009, 316(1): 311-322

[29]

FuW, HeXY, XuS, ChenW, LiY, LiB, SuLL, PingQ. Changes in nutrients and decay rate of Ginkgo biloba leaf litter exposed to elevated O3 concentration in urban area. PeerJ, 2018, 6 e4453

[30]

GaoYQ, YuanY, LiQK, KouL, FuXL, DaiXQ, WangHM. Mycorrhizal type governs foliar and root multi-elemental stoichiometries of trees mainly via root traits. Plant Soil, 2021, 460(1): 229-246

[31]

GeihsMA, MoreiraDC, López-MartínezG, MinariM, Ferreira-CravoM, Carvajalino-FernándezJM, Hermes-LimaM. Commentary: ultraviolet radiation triggers “preparation for oxidative stress” antioxidant response in animals: similarities and interplay with other stressors. Comp Biochem Physiol Part A Mol Integr Physiol, 2020, 239 110585

[32]

GuptaA, YadavDS, AgrawalSB, AgrawalM. Sensitivity of agricultural crops to tropospheric ozone: a review of Indian researches. Environ Monit Assess, 2022, 194(12): 894

[33]

GuptaA, YadavDS, AgrawalSB, AgrawalM. Individual effects of high temperature and tropospheric ozone on tomato: a review. J Plant Growth Regul, 2023, 42(3): 1421-1443

[34]

Hopkins WG (2016) A New View of Statistics [WWW Document]. URL http://newstats.org (accessed 10.4.24)

[35]

HoshikaY, AgathokleousE, MouraBB, PaolettiE. Ozone risk assessment with free-air controlled exposure (FACE) experiments: a critical revisit. Environ Res, 2024, 255 119215

[36]

HoshikaY, MouraBB, CotrozziL, NaliC, AlfarrajS, RennenbergH, PaolettiE. An assessment of ozone risk for date palm suggests that phytotoxic ozone dose nonlinearly affects carbon gain. Environ Pollut, 2024, 342 123143

[37]

ImtiazH, MirAR, CorpasFJ, HayatS. Impact of potassium starvation on the uptake, transportation, photosynthesis, and abiotic stress tolerance. Plant Growth Regul, 2023, 99(3): 429-448

[38]

IshfaqM, WangYQ, YanMW, WangZ, WuLQ, LiCJ, LiXX. Physiological essence of magnesium in plants and its widespread deficiency in the farming system of China. Front Plant Sci, 2022, 13 802274

[39]

IvattPD, EvansMJ, LewisAC. Suppression of surface ozone by an aerosol-inhibited photochemical ozone regime. Nat Geosci, 2022, 15: 536-540

[40]

JingT, LiJY, HeYD, ShankarA, SaxenaA, TiwariA, MaturiKC, SolankiMK, SinghV, EissaMA, DingZL, XieJH, AwasthiMK. Role of calcium nutrition in plant physiology: advances in research and insights into acidic soil conditions—a comprehensive review. Plant Physiol Biochem, 2024, 210 108602

[41]

KarabourniotisG, LiakopoulosG, NikolopoulosD, BrestaP, StavroulakiV, SumbeleS. “Carbon gain vs. water saving, growth vs. defence”: two dilemmas with soluble phenolics as a joker. Plant Sci, 2014, 227: 21-27

[42]

KhanF, SiddiqueAB, ShabalaS, ZhouMX, ZhaoCC. Phosphorus plays key roles in regulating plants' physiological responses to abiotic stresses. Plants, 2023, 12(15): 2861

[43]

KoerselmanW, MeulemanAFM. The vegetation N: P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol, 1996, 33(6): 1441-1450

[44]

KrohlingCA, EutrópioFJ, BertolaziAA, DobbssLB, CampostriniE, DiasT, RamosAC. Ecophysiology of iron homeostasis in plants. Soil Sci Plant Nutr, 2016, 62(1): 39-47

[45]

Lee JonesA, OrmondroydA, HayesF, JeffersES. Reflections of stress: Ozone damage in broadleaf saplings can be identified from hyperspectral leaf reflectance. Environ Pollut, 2024, 360 124642

[46]

LiL, WangXK, NiuJF, CuiJ, ZhangQQ, WanWX, LiuBJ. Effects of elevated atmospheric O3 concentrations on early and late leaf growth and elemental contents of Acer truncatum Bung under mild drought. Acta Ecol Sin, 2017, 37(1): 31-34

[47]

LiP, FengZZ, CatalayudV, YuanXY, XuYS, PaolettiE. A meta-analysis on growth, physiological, and biochemical responses of woody species to ground-level ozone highlights the role of plant functional types. Plant Cell Environ, 2017, 40(10): 2369-2380

[48]

LiS, YangY, WangHL, LiPW, LiK, RenLL, WangPY, LiBJ, MaoYH, LiaoH. Rapid increase in tropospheric ozone over Southeast Asia attributed to changes in precursor emission source regions and sectors. Atmos Environ, 2023, 304 119776

[49]

LimYJ, KwakMJ, LeeJ, KangD, JeSM, WooSY. Korean flowering cherry (Prunus × yedoensisMatsum.) response to elevated ozone: physiological traits and biogenic volatile organic compounds emission. Hortic Environ Biotechnol, 2024, 65(6): 1025-1042

[50]

LyuXP, LiK, GuoH, MorawskaL, ZhouBN, ZerenYZ, JiangF, ChenCH, GoldsteinAH, XuXB, WangT, LuX, ZhuT, QuerolX, ChataniS, LatifMT, SchuchD, SinhaV, KumarP, MullinsB, SeguelR, ShaoM, XueLK, WangN, ChenJM, GaoJ, ChaiFH, SimpsonI, SinhaB, BlakeDR. A synergistic ozone-climate control to address emerging ozone pollution challenges. One Earth, 2023, 6(8): 964-977

[51]

ManziniJ, HoshikaY, DantiR, MouraBB, PaolettiE, Della RoccaG. Ozone risk assessment of common cypress (Cupressus sempervirens L.) clones and effects of Seiridium cardinale infection. J Environ Sci, 2024, 151: 441-453

[52]

MatzekV, VitousekPM. N: P stoichiometry and protein: RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis. Ecol Lett, 2009, 12(8): 765-771

[53]

NakajiT, KobayashiT, KurohaM, OmoriK, MatsumotoY, YonekuraT, WatanabeK, UtriainenJ, IzutaT. Growth and nitrogen availability of red pine seedlings under high nitrogen load and elevated ozone. Water Air Soil Pollut Focus, 2004, 4(2): 277-287

[54]

PaolettiE, SicardP, HoshikaY, FaresS, BadeaO, PitarD, PopaI, AnavA, MouraBB, De MarcoA. Towards long-term sustainability of stomatal ozone flux monitoring at forest sites. Sustain Horiz, 2022, 2 100018

[55]

PaolettiE, PaganoM, ZhangL, BadeaO, HoshikaY. Allocation of nutrients and leaf turnover rate in poplar under ambient and enriched ozone exposure and soil nutrient manipulation. Biology, 2024, 13(4): 232

[56]

Pérez-HarguindeguyN, DíazS, VendraminiF, CornelissenJHC, GurvichDE, CabidoM. Leaf traits and herbivore selection in the field and in Cafeteria experiments. Austral Ecol, 2003, 28(6): 642-650

[57]

PerssonJ, FinkP, GotoA, HoodJM, JonasJ, KatoS. To be or not to be what you eat: regulation of stoichiometric homeostasis among autotrophs and heterotrophs. Oikos, 2010, 119: 741-751

[58]

QiZP, FangXY, XieYY, WangL, ZhangYW, ZhaoLG. Bioassay-guided isolation of anti-inflammatory constituents from Celtissinensis leaves. J Food Biochem, 2021, 45(1): e13580

[59]

QuerolX, MassaguéJ, AlastueyA, MorenoT, GangoitiG, MantillaE, DuéguezJJ, EscuderoM, MonfortE, Pérez García-PandoC, PetetinH, JorbaO, VázquezV, de la RosaJ, CamposA, MuñózM, MongeS, HervásM, JavatoR, CornideMJ. Lessons from the COVID-19 air pollution decrease in Spain: Now what?. Sci Total Environ, 2021, 779 146380

[60]

SchmidtSB, HustedS. The biochemical properties of manganese in plants. Plants, 2019, 8(10): 381

[61]

SebastianoM, MessinaS, MarascoV, CostantiniD. Hormesis in ecotoxicological studies: a critical evolutionary perspective. Curr Opin Toxicol, 2022, 29: 25-30

[62]

ShangB, FengZZ, LiP, CalatayudV. Elevated ozone affects C, N and P ecological stoichiometry and nutrient resorption of two poplar clones. Environ Pollut, 2018, 234: 136-144

[63]

ShashikumarA, BičárováS, LaurenceDR. The effect of ozone on pine forests in South-Eastern France from 2017 to 2019. J Forestry Res, 2023, 34(2): 301-315

[64]

ShenYB, PengY, ZhuXC, LiHM, ZhangLW, KongFL, WangJ, YuD. The phytochemicals and health benefits of Cyclocarya paliurus (Batalin) Iljinskaja. Front Nutr, 2023, 10: 1158158

[65]

ShiC, KitaoM, AgathokleousE, WatanabeM, TobitaH, YazakiK, KitaokaS, KoikeT. Foliar chemical composition of two oak species grown in a free-air enrichment system with elevated O3 and CO2. J Agric Meteorol, 2016, 72(1): 50-58

[66]

ShiC, WatanabeT, KoikeT. Leaf stoichiometry of deciduous tree species in different soils exposed to free-air O3 enrichment over two growing seasons. Environ Exp Bot, 2017, 138: 148-163

[67]

SicardP, AgathokleousE, De MarcoA, PaolettiE. Ozone-reducing urban plants: choose carefully. Science, 2022, 377(6606): 585

[68]

SinghAA, GhoshA, AgrawalM, AgrawalSB. Secondary metabolites responses of plants exposed to ozone: an update. Environ Sci Pollut Res Int, 2023, 30(38): 88281-88312

[69]

SkórkaM, SieprawskaA, TelkA. The implication of manganese surplus on plant cell homeostasis: a review. J Plant Growth Regul, 2023, 42(3): 1327-1341

[70]

TaibM, RezzakY, BouyazzaL, LyoussiB. Medicinal uses, phytochemistry, and pharmacological activities of Quercus species. Evid Based Complement Altern Med, 2020, 2020: 1920683

[71]

Tallmadge GK (1977) Ideabook: the joint dissemination review panel. U.S. Dept. of Health, Education and Welfare, National Institute of Education, U.S. Office of Education, Washington

[72]

ThorK. Calcium-nutrient and messenger. Front. Plant Sci, 2019, 10: 440

[73]

USDA (2024) Nuttall Oak [WWW Document]. https://www.srs.fs.usda.gov/pubs/misc/ag_654/volume_2/quercus/nutallii.htm

[74]

WallinG, KarlssonPE, SelldénG, OttossonS, MedinEL, PleijelH, SkärbyL. Impact of four years exposure to different levels of ozone, phosphorus and drought on chlorophyll, mineral nutrients, and stem volume of Norway spruce. Picea Abies Physiol Plant, 2002, 114(2): 192-206

[75]

WangT, XueLK, FengZZ, DaiJN, ZhangYN, TanY. Ground-level ozone pollution in China: a synthesis of recent findings on influencing factors and impacts. Environ Res Lett, 2022, 17(6): 063003

[76]

WangYT, WangYC, FengZZ, YuanXY, ZhaoY. The impacts of ambient ozone pollution on China’s wheat yield and forest production from 2010 to 2021. Environ Pollut, 2023, 330 121726

[77]

WangC, TangRJ, KouSH, XuXS, LuY, RauscherK, VoelkerA, LuanS. Mechanisms of calcium homeostasis orchestrate plant growth and immunity. Nature, 2024, 627(8003): 382-388

[78]

WolfFMMeta-analysis: quantitative methods for research synthesis, 1986, Beverly Hills, Sage Publications: 72p

[79]

XiaLL, LamSK, KieseR, ChenDL, LuoYQ, van GroenigenKJ, AinsworthEA, ChenJ, LiuSW, MaL, ZhuYH, Butterbach-BahlK. Elevated CO2 negates O3 impacts on terrestrial carbon and nitrogen cycles. One Earth, 2021, 4(12): 1752-1763

[80]

YanRS, WangHL, HuangC, AnJY, BaiHM, WangQ, GaoYQ, JingSG, WangYY, SuH. Impact of spatial scales of control measures on the effectiveness of ozone pollution mitigation in Eastern China. Sci Total Environ, 2024, 906 167521

[81]

YeH, LiC, YeW, ZengF, LiuF, LiuY, WangF, YeY, LinF, LiJYeH, LiC, YeW, ZengF. Medicinal angiosperms of Ulmaceae. Common Chinese Materia Medica: Volume 5, 2021, Singapore, Springer Nature : 61-86

[82]

YuanZY, ChenHYH. Decoupling of nitrogen and phosphorus in terrestrial plants associated with global changes. Nat Clim Change, 2015, 5: 465-469

[83]

ZhangYL, HanZY, LiXY, ZhangHL, YuanXY, FengZZ, WangP, MuZB, SongW, BlakeDR, YingQ, GeorgeC, ShengGY, PengPA, WangXM. Plants and related carbon cycling under elevated ground-level ozone: a mini review. Appl Geochem, 2022, 144 105400

[84]

ZhangK, XianL, ShangB, XuYS, FengZZ, AgathokleousE. Fluctuating ozone exposures caused trade-offs between vegetative growth and reproduction of two Chinese bean cultivars and ethylenediurea alleviated ozone phytotoxicities. J Environ Sci in Press, 2025

[85]

ZhouXY, YueX, TianCG. Responses of ecosystem productivity to anthropogenic ozone and aerosols at the 2060. Earth’s Futur, 2024, 12(1): E2023EF003781

[86]

ZhuangMH, LamSK, LiYC, ChenSL. Elevated tropospheric ozone affects the concentration and allocation of mineral nutrients of two bamboo species. Sci Total Environ, 2017, 577: 231-235

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