Photosynthetica X:X | DOI: 10.32615/ps.2026.016

Response of the photosynthetic apparatus of turfgrass varieties of perennial ryegrass and red fescue to naphthalene and fluoranthene contamination

P. DˇBROWSKI1, T. GNATOWSKI1, J. PRZYBYŁOWSKI2, M.J. MAŁUSZYŃSKI1, I. MAŁUSZYŃSKA1, B. PAWLU¦KIEWICZ1, H.M. KALAJI3
1 Department of Environmental Development and Remote Sensing, Warsaw University of Life Sciences, 02-776 Warsaw, Poland
2 Warsaw University of Life Sciences - SGGW, Faculty of Civil and Environmental Engineering, Interdepartmental Student Scientific Association of Ecoengineering, Warsaw University of Life Sciences, 02-776 Warsaw, Poland
3 Department of Botany and Plant Physiology, Warsaw University of Life Sciences, 02-776 Warsaw, Poland

The accumulation of polycyclic aromatic hydrocarbons (PAH) in urban soils poses a serious threat to plants. In this study, we compared the effects of naphthalene and fluoranthene on the photosynthetic apparatus of two lawn grass species: Lolium perenne L. (vars. Nira and Roadrunner) and Festuca rubra L. (var. Nimba). Compounds were applied to the substrate at concentrations of 20 and 40 mg kg-1(DM). Plant gas exchange and chlorophyll a fluorescence parameters were measured at 0, 240, and 480 h after their application. All treatments caused a progressive, time-dependent decline in the photosynthetic performance of the plants: net photosynthesis, transpiration rates, and stomatal conductance decreased. On the other hand, intercellular CO2 concentration (Ci) increased, indicating a shift from stomatal to nonstomatal limitations of photosynthesis. The performance index was shown to be a sensitive indicator of PAH phytotoxicity. Distinct patterns of photosystem damage were observed among the varieties, including antenna dissociation in Nimba, reaction centre destruction in Nira, and overall degradation of the photosynthetic apparatus in Roadrunner. Among the tested cultivars, Nimba (Festuca rubra) demonstrated the greatest overall tolerance to PAH-induced photosynthetic stress and is therefore recommended for use in contaminated urban landscapes.

Additional key words: nonstomatal limitation; performance index; phytotoxic stress; plant gas exchange; polycyclic aromatic hydrocarbons.

Received: March 22, 2026; Revised: May 27, 2026; Accepted: June 12, 2026; Prepublished online: July 14, 2026 

Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Ali-Taleshi M.S., Moeinaddini M., Riyahi-Bakhtiari A. et al.: A one-year monitoring of spatiotemporal variations of PM2.5-bound PAHs in Tehran, Iran: Source apportionment, local and regional sources origins and source-specific cancer risk assessment. - Environ. Pollut. 274: 115883, 2021.
    2. Aro E.-M., Virgin I., Andersson B.: Photoinhibition of photosystem II. Inactivation, protein damage and turnover. - BBA-Bioenergetics 1143: 113-134, 1993.
    3. Bussotti F., Gerosa G., Digrado A., Pollastrini M.: Selection of chlorophyll fluorescence parameters as indicators of photosynthetic efficiency in large scale plant ecological studies. - Ecol. Indic. 108: 105686, 2020.
    4. Cohen J.: Statistical Power Analysis for the Behavioral Sciences. 2nd Edition. Pp. 567. Routledge, New York 1988.
    5. D±browski P., Baczewska A.H., Pawlu¶kiewicz B. et al.: Prompt chlorophyll a fluorescence as a rapid tool for diagnostic changes in PSII structure inhibited by salt stress in perennial ryegrass. - J. Photoch. Photobio. B 157: 22-31, 2016.
    6. D±browski P., Małuszyńska I., Małuszyński M.J. et al.: Photosynthetic efficiency of plants as an indicator of tolerance to petroleum-contaminated soils. - Sustainability 16: 10811, 2024.
    7. Digrado A., Bachy A., Mozaffar A. et al.: Long-term measurements of chlorophyll a fluorescence using the JIP-test show that combined abiotic stresses influence the photosynthetic performance of the perennial ryegrass (Lolium perenne) in a managed temperate grassland. - Physiol. Plantarum 161: 355-371, 2017.
    8. Farquhar G.D., Sharkey T.D.: Stomatal conductance and photosynthesis. - Annu. Rev. Plant Biol. 33: 317-345, 1982.
    9. Fismes J., Perrin-Ganier C., Emperor-Bissonnet P., Morel J.L.: Soil-to-root transfer and translocation of polycyclic aromatic hydrocarbons by vegetables grown on industrial contaminated soils. - J. Environ. Qual. 31: 1649-1656, 2002.
    10. Flexas J., Ribas-Carbó M., Diaz-Espejo A. et al.: Mesophyll conductance to CO2: current knowledge and future prospects. -Plant Cell Environ. 31: 602-621, 2008.
    11. Gawryluk A., Krzyszczak J.: Effects of polycyclic aromatic hydrocarbons on germination and initial growth of selected lawn grass species in soil polluted with PAHs. - J. Ecol. Eng. 25: 175-186, 2024.
    12. Habibi G., Vaziri A.: High salicylic acid concentration alters the electron flow associated with photosystem II in barley. - Acta Agric. Slov. 109: 393-402, 2017.
    13. Jajoo A., Mekala N.R., Tomar R.S. et al.: Inhibitory effects of polycyclic aromatic hydrocarbons (PAHs) on photosynthetic performance are not related to their aromaticity. - J. Photoch. Photobio. B 137: 151-155, 2014.
    14. Joffe R., Berthe A., Jolivet Y., Gandin A.: The response of mesophyll conductance to ozone-induced oxidative stress is genotype-dependent in poplar. - J. Exp. Bot. 73: 4850-4866, 2022.
    15. Kalaji H.M., Jajoo A., Oukarroum A. et al.: Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. - Acta Physiol. Plant. 38: 102, 2016.
    16. Kalaji H.M., Schansker G., Brestic M. et al.: Frequently asked questions about chlorophyll fluorescence, the sequel. - Photosynth. Res. 132: 13-66, 2017.
    17. Kassambara A., Mundt F.: factoextra: Extract and Visualize the Results of Multivariate Data Analyses. R package version 1.0.7, 2020. Available at: https://CRAN.R-project.org/package=factoextra.
    18. Kreslavski V.D., Lankin A.V., Vasilyeva G.K. et al.: Effects of polyaromatic hydrocarbons on photosystem II activity in pea leaves. - Plant Physiol. Biochem. 81: 135-142, 2014.
    19. Kummerová M., Krulová J., Zezulka ©., Tříska J.: Evaluation of fluoranthene phytotoxicity in pea plants by Hill reaction and chlorophyll fluorescence. - Chemosphere 65: 489-496, 2006.
    20. LCpro+ Photosynthesis System: Operator's Manual. ADC BioScientific Ltd., Hoddesdon 2007.
    21. Lê S., Josse J., Husson F.: FactoMineR: An R Package for Multivariate Analysis. - J. Stat. Softw. 25: 1-18, 2008.
    22. Lichtenthaler H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. - Method. Enzymol. 148: 350-382, 1987.
    23. Lichtenthaler H.K.: Vegetation stress: An introduction to the stress concept in plants. - J. Plant Physiol. 148: 4-14, 1996.
    24. Małuszyński M.J., Pawlu¶kiewicz B., Gnatowski T. et al.: The effect of petroleum-derived compounds in soil on microbiological activity and the physiological state of plants. - Appl. Sci. 16: 2076, 2026.
    25. Marenco R.A., Siebke K., Farquhar G.D., Ball M.C.: Hydraulically based stomatal oscillations and stomatal patchiness in Gossypium hirsutum. - Funct. Plant Biol. 33: 1103-1113, 2006.
    26. Márquez D.A., Gardner A., Busch F.A.: Navigating challenges in interpreting plant physiology responses through gas exchange results in stressed plants. - Plant Ecophysiol. 1: 2, 2025.
    27. Molina L., Segura A.: Biochemical and metabolic plant responses toward polycyclic aromatic hydrocarbons and heavy metals present in atmospheric pollution. - Plants-Basel 10: 2305, 2021.
    28. Nakagawa S., Cuthill I.C.: Effect size, confidence interval and statistical significance: a practical guide for biologists. - Biol. Rev. 82: 591-605, 2007.
    29. Peak D., Hogan M.T., Mott K.A.: Stomatal patchiness and cellular computing. - PNAS 120: e2220270120, 2023.
    30. Posit Team: RStudio: Integrated Development Environment for R. Posit Software, PBC, Boston 2024. Available at: http://www.posit.co/.
    31. Quinn G.P., Keough M.J.: Experimental Design and Data Analysis for Biologists. Pp. 553. Cambridge University Press, Cambridge 2002.
    32. R Core Team: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna 2024. Available at: https://www.R-project.org/.
    33. Rastogi A., Kovar M., He M. et al.: JIP-test as a tool to identify salinity tolerance in sweet sorghum genotypes. - Photosynthetica 58: 518-528, 2020.
    34. Richardson J.T.E.: Eta squared and partial eta squared as measures of effect size in educational research. - Educ. Res. Rev. 6: 135-147, 2011.
    35. Rodríguez A.A., Vilas J.M., Sartore G.D. et al.: Field and genetic evidence support the photosynthetic performance index (PIABS) as an indicator of rice grain yield. - Plant Physiol. Biochem. 201: 107897, 2023.
    36. Savvides A.M., Fotopoulos V.: Two inexpensive and non-destructive techniques to correct for smaller-than-gasket leaf area in gas exchange measurements. - Front. Plant Sci. 9: 548, 2018.
    37. Sikkema J., de Bont J.A.M., Poolman B.: Mechanisms of membrane toxicity of hydrocarbons. - Microbiol. Rev. 59: 201-222, 1995.
    38. Smolewska M.E., Krasowska M., Piekut J. et al.: Assessment of PAH content in soil and aboveground parts of Lolium perenne L. next to communication arteries of the urban agglomeration. - Stud. Quat. 39: 5-13, 2022.
    39. Strasser R.J., Tsimilli-Michael M.: Stress in plants, from daily rhythm to global changes, detected and quantified by the JIP-test. - Chimie Nouvelle 75: 3321-3326, 2001.
    40. Strasser R.J., Tsimilli-Michael M., Srivastava A.: Analysis of the chlorophyll a fluorescence transient. - In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 321-362. Springer, Dordrecht 2004.
    41. Terashima I.: Anatomy of non-uniform leaf photosynthesis. - Photosynth. Res. 31: 195-212, 1992.
    42. Terashima I., Wong S.-C., Osmond C.B., Farquhar G.D.: Characterisation of non-uniform photosynthesis induced by abscisic acid in leaves having different mesophyll anatomies. -Plant Cell Physiol. 29: 385-394, 1988.
    43. Tomar R.S., Jajoo A.: Alteration in PSII heterogeneity under the influence of polycyclic aromatic hydrocarbon (fluoranthene) in wheat leaves (Triticum aestivum). - Plant Sci. 209: 58-63, 2013.
    44. Tomar R.S., Jajoo A.: Fluoranthene, a polycyclic aromatic hydrocarbon, inhibits light as well as dark reactions of photosynthesis in wheat (Triticum aestivum). - Ecotox. Environ. Safe. 109: 110-115, 2014.
    45. Tomar R.S., Jajoo A.: PSI becomes more tolerant to fluoranthene through the initiation of cyclic electron flow. - Funct. Plant Biol. 44: 978-984, 2017.
    46. Tsimilli-Michael M.: Revisiting JIP-test: An educative review on concepts, assumptions, approximations, definitions and terminology. - Photosynthetica 58: 275-292, 2020.
    47. Van Huylenbroeck J.M., Lootens P., Van Bockstaele E.: Photosynthetic characteristics of perennial ryegrass and red fescue turf-grass cultivars. - Grass Forage Sci. 54: 267-274, 1999.
    48. Váňová L., Kummerová M., Klemą M., Zezulka ©.: Fluoranthene influences endogenous abscisic acid level and primary photosynthetic processes in pea (Pisum sativum L.) plants in vitro. - Plant Growth Regul. 57: 39-47, 2009.
    49. Wickham H.: ggplot2: Elegant Graphics for Data Analysis. 2nd Edition. Pp. 260. Springer, Cham 2016.
    50. Zeng Y., Wang S., Huang F. et al.: Fate of polycyclic aromatic hydrocarbons in the phytoremediation of different hydrocarbon contaminated soils with cotton, ryegrass, tall fescue, and wheat. - Front. Plant Sci. 16: 1550234, 2025.
    51. ®ivčák M., Brestič M., Oląovská K., Slamka P.: Performance index as a sensitive indicator of water stress in Triticum aestivum L. - Plant Soil Environ. 54: 133-139, 2008.

    Return