Plant Soil Environ., 2025, 71(9):666-679 | DOI: 10.17221/328/2025-PSE

Species-specific responses of wheat and maize to thallium stress under elevated CO2: effects on yield, photosynthesis, and metabolismOriginal Paper

Samy Selim Abdelsalam1, Soad K. Al Jaouni2, Seham M. Hamed3, Emad A. Alsherif4, Afrah E. Mohammed5,6, Modhi O. Alotaibi5, Danyah A. Aldailami7, Wael A. Obaid8
1 Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, Jouf University, Sakaka, Saudi Arabia
2 Department of Haematology/Oncology, Chair of Prophetic Medicine Application, Faculty of Medicine, King Abdulaziz University and Hospital, Jeddah, Saudi Arabia
3 Department of Biology, College of Science, Imam Mohammad Ibn Saud Islamic University (IMSIU), Riyadh, Saudi Arabia
4 Department of Botany and Microbiology, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt
5 Department of Biology, College of Science, Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia
6 Microbiology and Immunology Unit, Natural and Health Sciences Research Centre, Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia
7 Public Health Department, College of Health Sciences, Saudi Electronic University, Riyadh, Saudi Arabia
8 Biology Department, College of Science, Taibah University, Al-Madinah Al-Munawwarah, Saudi Arabia

Heavy metal stress inhibits plant growth, but this impact is less studied and pronounced under climate change conditions. The present study investigates the physiological, biochemical, and agronomic responses of wheat (C3) and maize (C4) exposed to varying thallium (Tl) stress (60 and 120 mg/kg) under ambient (aCO2) and elevated (eCO2, 710 µmol/mol) CO2 levels. High Tl exposure markedly reduced grain yield by 58% in wheat and 68% in maize at 120 mg/kg under aCO2. However, eCO2 partially offset the negative effects, increasing yield by ~20% in wheat and 36% in maize at 60 mg/kg Tl. eCO2 enhanced photosynthetic activity under eCO2, which increased the accumulation of soluble sugars under TI stress. These provide carbon skeletons for the synthesis of primary metabolites such as amino acids, organic acids and fatty acids. Although total fatty acid content declined under stress, the metabolic crosstalk initiated by improved photosynthesis and sugar availability enables plants to maintain key fatty acids (such as palmitic, linolenic, and oleic acids) essential for membrane stability and function. Amino acids, especially proline and cysteine, accumulated significantly under Tl stress. These primary metabolites, in turn, feed into secondary metabolic pathways, promoting the formation of phenolic acids and flavonoids that enhance antioxidant defence and stress tolerance. This metabolic cascade explains eCO2’s capacity to alleviate TI stress and improve crop performance, and underscores the value of leveraging eCO2 environments to support agricultural productivity and food security under challenging conditions.

Keywords: C3 and C4 plants; environmental toxicity; physiological responses; Triticum aestivum L.; Zea mays L.

Received: July 26, 2025; Revised: September 17, 2025; Accepted: September 18, 2025; Prepublished online: September 25, 2025; Published: September 26, 2025  Show citation

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Abdelsalam SS, Al Jaouni SK, Hamed SM, Alsherif EA, Mohammed AE, Alotaibi MO, et al.. Species-specific responses of wheat and maize to thallium stress under elevated CO2: effects on yield, photosynthesis, and metabolism. Plant Soil Environ. 2025;71(9):666-679. doi: 10.17221/328/2025-PSE.
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References

  1. AbdElgawad H., Korany S.M., Hagagy N., Khanghahi M.Y., Reyad A.M., Crecchio C., Zakri A.M., Alsherif E.A., Bakkar M.R. (2023): Biochemical and pharmaceutical traits of Marrubium vulgare L. plants treated with plant growth-promoting bacteria and elevated CO2. 3 Biotech, 13: 412. Go to original source... Go to PubMed...
  2. AbdElgawad H., Zinta G., Hamed B.A., Selim S., Beemster G.T.S., Hozzein W.N., Wadaan M.A.M., Asard H., Abuelsoud W. (2020): Maize roots and shoots show distinct profiles of oxidative stress and antioxidant defense under heavy metal toxicity. Environmental Pollution, 258: 113705. Go to original source... Go to PubMed...
  3. AbdElgawad H., De Vos D., Zinta G. (2015): Grassland species differentially regulate proline concentrations under future climate conditions: an integrated biochemical and modelling approach. New Phytologist, 208: 354-369. Go to original source... Go to PubMed...
  4. Abdel-Mawgoud M., Bouqellah N.A., Korany S.M., Reyad A.M., Hassan A.H.A., Alsherif E.A., AbdElgawad H. (2023): Arbuscular mycorrhizal fungi as an effective approach to enhance the growth and metabolism of soybean plants under thallium (TI) toxicity. Plant Physiology and Biochemistry, 203: 108077. Go to original source... Go to PubMed...
  5. Afzal S., Chaudhary N., Singh N.K. (2021): Role of soluble sugars in metabolism and sensing under abiotic stress. In: Aftab T., Hakeem K.R. (eds.): Plant Growth Regulators: Signalling under Stress Conditions. Cham, Springer, 305-334. ISBN: 978-3-030-61153-8 Go to original source...
  6. Albqmi M., Yaghoubi Khanghahi M., Selim S., Al-Sanea M.M., Alnusaire T.S., Almuhayawi M.S., Al Jaouni S.K., Hussein S., Warrad M., AbdEl-gawad H. (2023a): Positive interaction of selenium nanoparticles and olive solid waste on vanadium-stressed soybean plant. Agriculture, 13: 426. Go to original source...
  7. Albqmi M., Selim S., Yaghoubi Khanghahi M., Crecchio C., Al-Sanea M.M., Alnusaire T.S., Almuhayawi M.S., Al Jaouni S.K., Hussein S., Warrad M., AbdElgawad H. (2023b): Chromium (VI) toxicity and active tolerance mechanisms of wheat plant treated with plant growth-promoting actinobacteria and olive solid waste. ACS Omega, 8: 32458-32467. Go to original source... Go to PubMed...
  8. Alsherif E.A., Hajjar D., Aldilami M., AbdElgawad H. (2023): Physiological and biochemical responses of wheat to synergistic effects of selenium nanoparticles and elevated CO2 conditions. Frontiers in Plant Science, 14: 1183185. Go to original source... Go to PubMed...
  9. Bamrah R.K., Vijayan P., Karunakaran C., Muir D., Hallin E., Stobbs J., Goetz B., Nickerson M., Tanino K., Warkentin T.D. (2019): Evaluation of X-ray fluorescence spectroscopy as a tool for nutrient analysis of pea seeds. Crop Science, 59: 2689-2700. Go to original source...
  10. Blandino M., Badeck F.W., Giordano D., Marti A., Rizza F., Scarpino V., Vaccino P. (2020): Elevated CO2 impact on common wheat (Triticum aestivum L.) yield, whole meal quality, and sanitary risk. Journal of Agricultural and Food Chemistry, 68: 10574-10585. Go to original source... Go to PubMed...
  11. Broberg M.C., Högy P., Feng Z., Pleijel H. (2019): Effects of elevated CO2 on wheat yield: non-linear response and relation to site productivity. Agronomy, 9: 243. Go to original source...
  12. Dubey S.K., Tripathi S.K., Pranuthi G. (2015): Effect of elevated CO2 on wheat crop: mechanism and impact. Critical Reviews in Environmental Science and Technology, 45: 2283-2304. Go to original source...
  13. Elbasan F., Ozfidan-Konakci C., Yildiztugay E., Kucukoduk M. (2020): Rare-earth element scandium improves stomatal regulation and enhances salt and drought stress tolerance by up-regulating antioxidant responses of Oryza sativa. Plant Physiology and Biochemistry, 152: 157-169. Go to original source... Go to PubMed...
  14. Galtier N., Foyer C.H., Murchie E. (1995): Effects of light and atmosphere CO2 enrichment on photosynthetic carbon partitioning and carbon/nitrogen ratios in tomato (Lycopersicon esculentum L.) plants overexpressing sucrose phosphate synthase. Journal of Experimental Botany, 46: 1335-1344. Go to original source...
  15. Gowik U., Westhoff P. (2011): The path from C3 to C4 photosynthesis. Plant Physiology, 155: 56-63. Go to original source... Go to PubMed...
  16. Grote U., Fasse A., Nguyen T.T., Erenstein O. (2021): Food security and the dynamics of wheat and maize value chains in Africa and Asia. Frontiers in Sustainable Food Systems, 4: 617009. Go to original source...
  17. Hagagy N., AbdElgawad H. (2024): Rapeseed plant: biostimulation effects of plant growth-promoting Actinobacteria on metabolites and antioxidant defence system under elevated CO2 conditions. Journal of the Science of Food and Agriculture, 104: 51-62. Go to original source... Go to PubMed...
  18. Hasanuzzaman M., Nahar K., Anee T.I., Fujita M. (2017): Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiology and Molecular Biology of Plants, 23: 249-268. Go to original source... Go to PubMed...
  19. Hrubý M., Cígler P., Kuzel S. (2002): Contribution to understanding the mechanism of titanium action in plants. Journal of Plant Nutrition, 25: 577-598. Go to original source...
  20. Jamali M., Bakhshandeh E., Yaghoubi Khanghahi M., Crecchio C. (2021): Metadata analysis to evaluate environmental impacts of wheat residues burning on soil quality in developing and developed countries. Sustainability, 13: 6356. Go to original source...
  21. Kaur H., Kumar A., Choudhary A., Sharma S., Choudhary D.R., Mehta S. (2023): Chapter 3 - Effect of elevated CO2 on plant growth, active constituents, and production. In: Azamal H. (ed.): Plants and their Interaction to Environmental Pollution. Amsterdam, Elsevier, 61-77. Go to original source...
  22. McCleary B.V., Sheehan H. (1987): Measurement of cereal α-amylase: a new assay procedure. Journal of Cereal Science, 6: 237-251. Go to original source...
  23. Mereu V., Gallo A., Trabucco A., Carboni G., Spano D. (2021): Modeling high-resolution climate change impacts on wheat and maize in Italy. Climate Risk Management, 33: 100339. Go to original source...
  24. Naz M., Afzal M.R., Raza M.A., Pandey S., Qi S., Dai Z., Du D. (2024): Calcium (Ca2+) signaling in plants: a plant stress perspective. South African Journal of Botany, 169: 464-485. Go to original source...
  25. Obaid W.A., Selim S., Hamed S.M., Alsherif E.A., Korany S.M., Sonbol H., Aldailami D.A., Al Jaouni S.K. (2025): Wheat (C3) and maize (C4) adaptive responses to soil thallium toxicity under elevated CO2 conditions. Plant, Soil and Environment, 71: 534-552. Go to original source...
  26. Patra M., Bashir O., Amin T., Wani A.W., Shams R., Chaudhary K.S., Mirza A.A., Manzoor S. (2023): A comprehensive review on functional beverages from cereal grains-characterization of nutraceutical potential, processing technologies and product types. Heliyon, 9: e16804. Go to original source... Go to PubMed...
  27. Porra R.J. (2002): The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynthesis Research, 73: 149-156. Go to original source... Go to PubMed...
  28. Riaz M.W., Wu T., Hussain Q., Haider F.U., Jiang W., Shao Q., Manzoor M.A., Xing B. (2024): Heavy metal stress in medicinal plants: detoxification mechanisms, antioxidants, and implications for human health. Journal of Soil Science and Plant Nutrition, 24: 1823-1856. Go to original source...
  29. Sahu R., Mandal R., Das P., Ashraf G.J., Dua T.K., Paul P., Nandi G., Khanra R. (2023): The bioavailability, health advantages, extraction method, and distribution of free and bound phenolics of rice, wheat, and maize: a review. Food Chemistry Advances, 3: 100484. Go to original source...
  30. Santos J.F., Dirk L.M.A., Downie A.B., Sanches M.F.G., Vieira R.D. (2017): Reciprocal effect of parental lines on the physiological potential and seed composition of corn hybrid seeds. Seed Science Research, 27: 206-216. Go to original source...
  31. Sekhar K.M., Sreeharsha R.V., Reddy A.R. (2015): Differential responses in photosynthesis, growth and biomass yields in two mulberry genotypes grown under elevated CO2 atmosphere. Journal of Photochemistry and Photobiology B: Biology, 151: 172-179. Go to original source... Go to PubMed...
  32. Shabbaj I.I., Abdelgawad H., Balkhyour M.A., Tammar A., Madany M.M.Y. (2022): Elevated CO2 differentially mitigated oxidative stress induced by indium oxide nanoparticles in young and old leaves of C3 and C4 crops. Antioxidants, 11: 308. Go to original source... Go to PubMed...
  33. Sreeharsha R.V., Mudalkar S., Sengupta D. (2019): Mitigation of drought-induced oxidative damage by enhanced carbon assimilation and an efficient antioxidative metabolism under high CO2 environment in pigeonpea (Cajanus cajan L.). Photosynthesis Research, 139: 425-439. Go to original source... Go to PubMed...
  34. Srivastava J., Chandra H., Nautiyal A.R., Kalra S.J. (2012): Response of C3 and C4 plant systems exposed to heavy metals for phytoextraction at elevated atmospheric CO2 and at elevated temperature. Environmental Contamination, 1: 3-16. Go to original source...
  35. Sturm K., Koron D., Stampar F. (2003): The composition of fruit of different strawberry varieties depending on maturity stage. Food Chemistry, 83: 417-422. Go to original source...
  36. Thalmann M., Santelia D. (2017): Starch as a determinant of plant fitness under abiotic stress. New Phytologist, 214: 943-951. Go to original source... Go to PubMed...
  37. Thalmann M., Pazmino D., Seung D., Horrer D., Nigro A., Meier T., Kölling K., Pfeifhofer H.W., Zeeman S.C., Santelia D. (2016): Regulation of leaf starch degradation by abscisic acid is important for osmotic stress tolerance in plants. The Plant Cell, 28: 1860-1878. Go to original source... Go to PubMed...
  38. Tian W., Su C., Zhang N., Zhao Y., Tang L. (2024): Simulation of the physiological and photosynthetic characteristics of C3 and C4 plants under elevated temperature and CO2 concentration. Ecological Modelling, 495: 110805. Go to original source...
  39. Torras-Claveria L., Berkov S., Codina C. (2014): Metabolomic analysis of bioactive Amaryllidaceae alkaloids of ornamental varieties of Narcissus by GC-MS combined with k-means cluster analysis. Industrial Crops and Products, 56: 211-222. Go to original source...
  40. Upchurch R.G. (2008): Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnology Letters, 30: 967-977. Go to original source... Go to PubMed...
  41. Wang L., Feng Z., Schjoerring J.K. (2013): Effects of elevated atmospheric CO2 on physiology and yield of wheat (Triticum aestivum L.): a meta-analytic test of current hypotheses. Agriculture, Ecosystems and Environment, 178: 57-63. Go to original source...
  42. Wang X., Lv P., Zhang F., Wang W., Liu X., Zhang Q., Mu J., Huang X., Bai L., Dai J. (2025a): Heavy metal accumulation in maize and wheat in acidic soil: a comparative study. Sustainability, 17: 2084. Go to original source...
  43. Wang L.N., Wang W.C., Liao K., Xu L.J., Xie D.X., Xie R.H., Xiao S. (2025b): Survival mechanisms of plants under hypoxic stress: physiological acclimation and molecular regulation. Journal of Integrative Plant Biology, 67: 440-454. Go to original source... Go to PubMed...
  44. Yaghoubi K.M., Pirdashti H., Rahimian H., Nematzadeh G.A., Ghajar Sepanlou M., Salvatori E., Crecchio C. (2019): Evaluation of leaf photosynthetic characteristics and photosystem II photochemistry of rice (Oryza sativa L.) under potassium solubilising bacteria (KSB) inoculation. Pho-tosynthetica, 57: 500-511. Go to original source...
  45. Yaghoubi K.M., AbdElgawad H., Verbruggen E., Korany S.M., Alsherif E.A., Beemster G.T.S. (2022): Biofertilization with a consortium of growth-promoting bacterial strains improves the nutritional status of wheat grain under control, drought, and salinity stress conditions. Physiologia Plantarum, 174: e13800. Go to original source... Go to PubMed...
  46. Yoshida Y., Marubodee R., Ogiso-Tanaka E., Iseki K., Isemura T., Takahashi Y., Tomooka N. (2016): Salt tolerance in wild relatives of adzuki bean, Vigna angularis (Willd.) Ohwi et Ohashi. Genetic Resources and Crop Evolution, 63: 627-637. Go to original source...
  47. Zhang Q., Zhang J., Shen J., Silva A., Dennis D.A., Barrow C.J. (2006): A simple 96-well microplate method for estimation of total polyphenol content in seaweeds. Journal of Applied Phycology, 18: 445-450. Go to original source...
  48. Zinta G., AbdElgawad H., Peshev D. (2018): Dynamics of metabolic responses to periods of combined heat and drought in Arabidopsis thaliana under ambient and elevated atmospheric CO2. Journal of Experimental Botany, 69: 2159-2170. Go to original source... Go to PubMed...

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