Photosynthetic efficiency and gene expression responses of maize (Zea mays L.) seedlings to diverse abiotic stresses

Aghaie, P. and Tafreshi, S.A.H. (2020) “Central role of 70-kDa heat shock protein in adaptation of plants to drought stress,” Cell Stress Chaperones, 25, pp. 1071–1081. Available at: https://doi.org/10.1007/s12192-020-01144-7.

Ahluwalia, O., Singh, P.C. and Bhatia, R. (2021) “A review on drought stress in plants: Implications, mitigation and the role of plant growth promoting rhizobacteria,” Resources, Environment and Sustainability, 5, 100032. Available at: https://doi.org/10.1016/j.resenv.2021.100032.

Baker, N.R. and Rosenqvist, E. (2004) “Applications of chlorophyll fluorescence can improve crop production strategies: An examination of future possibilities,” Journal of Experimental Botany, 55, pp. 1607–1621. Available at: https://doi.org/10.1093/jxb/erh196.

Banti, V. et al. (2010) “The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis,” Plant Physiology, 152, pp. 1471–1483. Available at: https://doi.org/10.1104/pp.109.149815.

Baruah, N. et al. (2023) “Phytotoxic responses and plant tolerance mechanisms to cadmium toxicity,” Journal of Soil Science and Plant Nutrition, 23, pp. 4805–4826. Available at: https://doi.org/10.1007/s42729-023-01525-8.

Bhattacharya, A. (2022) “Effect of low temperature stress on photosynthesis and allied traits: A review,” in Bhattacharya, A. (ed.) Physiological processes in plants under low temperature stress. Singapore: Springer, pp. 199–297. Available at: https://doi.org/10.1007/978-981-16-9037-2_3.

Bionda, T. et al. (2016) “Eukaryotic Hsp70 chaperones in the intermembrane space of chloroplasts,” Planta, 243, pp. 733–747. Available at: https://doi.org/10.1007/s00425-015-2440-z.

Björkman, O. and Demmig, B. (1987) “Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins,” Planta, 170, pp. 489–504. Available at: https://doi.org/10.1007/BF00402983.

Brestič, M. et al. (2015) “Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines,” Photosynthetic Research, 125, pp. 151–166. Available at: https://doi.org/10.1007/s11120-015-0093-1.

Chalker-Scott, L. (1999) “Environmental significance of anthocyanins in plant stress responses,” Photochemistry and Photobiology, 70, pp. 1–9. Available at: https://doi.org/10.1111/j.1751-1097.1999. tb01944.x.

Chen, J. et al. (2017) “Arabidopsis WRKY46, WRKY54, and WRKY70 transcription factors are involved in brassinosteroid-regulated plant growth and drought responses,” Plant Cell, 29, pp. 1425–1439. Available at: https://doi.org/10.1105/tpc.17.00364.

Chen, J. et al. (2021) “Effects of drought on the relationship between photosynthesis and chlorophyll fluorescence for maize,” IEEE Journal of Selected Topics in Applied Earth Observations and Remote Sensing, 14, pp. 11148–11161. Available at: https://doi.org/10.1109/JSTARS.2021.3123111.

Chtouki, M. et al. (2021) “Effect of cadmium and phosphorus interaction on tomato: Chlorophyll a fluorescence, plant growth, and cadmium translocation,” Water Air Soil Pollution, 232, 84. Available at: https://doi.org/10.1007/s11270-021-05038-x.

Dąbrowski, P. et al. (2024a) “Photosynthetic efficiency of plants as an indicator of tolerance to petroleum-contaminated soils,” Sustainability, 16, 10811. Available at: https://doi.org/10.3390/su162410811.

Dąbrowski, P. et al. (2024b) “Relationship between photosynthetic performance and yield loss in winter oilseed rape (Brassica napus L.) under frost conditions,” Photosynthetica, 62, pp. 240–251. Available at: https://doi.org/10.32615/ps.2024.025.

Dąbrowski, P. et al. (2024c) “Photosynthetic performance and yield losses of winter rapeseed (Brassica napus L. var. napus) caused by simulated hail,” Plants, 13, 1785. Available at: https://doi.org/10.3390/plants13131785.

Dinç, E. et al. (2012) “The Chl a fluorescence intensity is remarkably insensitive to changes in the chlorophyll content of the leaf as long as the Chl a/b ratio remains unaffected,” Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1817, pp. 770–779. Available at: https://doi.org/10.1016/j.bbabio.2012.02.003.

Distéfano, A.M. et al. (2017) “Heat stress induces ferroptosis-like cell death in plants,” Journal of Cell Biology, 216, pp. 463–476. Available at: https://doi.org/10.1083/jcb.201605110.

Farooq, M. et al. (2009) “Plant drought stress: Effects, mechanisms and management,” Agronomy for Sustainable Development, 29, pp. 185–212. Available at: https://doi.org/10.1051/agro:2008021.

Farooq, M. et al. (2024) “Real-time expression and in silico characterization of pea genes involved in salt and water-deficit stress,” Molecular Biology Reports, 51, 18. Available at: https://doi.org/10.1007/s11033-023-09064-2.

Forestan, C. et al. (2016) “Stress-induced and epigenetic-mediated maize transcriptome regulation study by means of transcriptome reannotation and differential expression analysis,” Scientific Reports 6, 30446. Available at: https://doi.org/10.1038/srep30446.

Ghosh, M. and Singh, S.P. (2005) “A review on phytoremediation of heavy metals and utilization of its byproducts,” Applied Ecology and Environmental Research, 3, pp. 1–18. Available at: https://doi.org/10.15666/aeer/0301_001018.

Gu, L. et al. (2019) “Sun-induced chlorophyll fluorescence and its importance for biophysical modeling of photosynthesis based on light reactions,” New Phytologist, 223, pp. 1179–1191. Available at: https://doi.org/10.1111/nph.15796.

Helm, L.T. et al. (2020) “Solar-induced chlorophyll fluorescence and short-term photosynthetic response to drought,” Ecological Applications, 30, e02101. Available at: https://doi.org/10.1002/eap.2101.

Holm, S.A. (1979) “Simple sequentially rejective multiple test procedure,” Scandinavian Journal of Statistics, 6, pp. 65–70. Available at: https://www.jstor.org/stable/4615733 (Accessed: April 02, 2025).

Hu, X. et al. (2010) “Heat shock protein 70 regulates the abscisic acid-induced antioxidant response of maize to combined drought and heat stress,” Plant Growth Regulators, 60, pp. 225–235. Available at: https://doi.org/10.1007/s10725-009-9436-2.

Iqbal, H. et al. (2020) “Improving heat stress tolerance in late planted spring maize by using different exogenous elicitors,” Chilean Journal of Agricultural Research, 80, pp. 30–40. Available at: https://doi.org/10.4067/S0718-58392020000100030.

Iqbal, S. et al. (2020) “The response of maize physiology under salinity stress and its coping strategies,” in A. Hossain (ed.) Plant stress physiology. London: IntechOpen Limited, pp. 1–25. Available at: https://doi.org/10.5772/intechopen.92213.

Janská, A. et al. (2010) “Cold stress and acclimation – what is important for metabolic adjustment?,” Plant Biology, 12, pp. 395–405. Available at: https://doi.org/10.1111/j.1438-8677.2009.00299.x.

Jiao, P. et al. (2022) “Integration of mRNA and microRNA analysis reveals the molecular mechanisms underlying drought stress tolerance in maize (Zea mays L.),” Frontiers in Plant Science, 13, 932667. Available at: https://doi.org/10.3389/fpls.2022.932667.

Jin, H. et al. (2019) “Maize leaves drought-responsive genes revealed by comparative transcriptome of two cultivars during the filling stage,” PLOS ONE, 14, e0223786. Available at: https://doi.org/10.1371/journal.pone.0223786.

Kalaji, M.H. and Guo, P. (2008) “Chlorophyll fluorescence: A useful tool in barley plant breeding programs,” in A. Sanchez, S.J. Gutierrez (eds.) Photochemistry research progress. New York: Nova Publishers, pp. 439–463.

Klimešová, J. et al. (2021) “Transpiration and water use efficiency of maize in different soil moisture conditions,” Acta Horticulturae et Regiotecturae, 24, pp. 105–109. Available at: https://doi.org/10.2478/ahr-2021-0031.

Klimešová, J., Holková, L. and Středa, T. (2017) “The expression of dehydrin genes and the intensity of transpiration in drought-stressed maize plants,” Cereal Research Communications, 45, pp. 355–368. Available at: https://doi.org/10.1556/0806.45.2017.017.

Kohli, S.K. et al. (2017) “Role of salicylic acid in heavy metal stress tolerance: Insight into underlying mechanism,” in R. Nazar, N. Iqbal and N. Khan (eds.) Salicylic acid: A multifaceted hormone. Singapore: Springer, pp. 123–144. Available at: https://doi.org/10.1007/978-981-10-6068-7_7.

Kosová, K. et al. (2025) “How to survive mild winters: Cold acclimation, deacclimation, and reacclimation in winter wheat and barley,” Plant Physiology and Biochemistry, 220, 109541. Available at: https://doi.org/10.1016/j.plaphy.2025.109541.

Kosová, K. Vítámvás, P. and Prášil, I.T (2014) “Proteomics of stress responses in wheat and barley – search for potential protein markers of stress tolerance,” Frontiers in Plant Science, 5, 711. Available at: https://doi.org/10.3389/fpls.2014.00711.

Kozeko, L. (2021) “Different roles of inducible and constitutive HSP70 and HSP90 in tolerance of Arabidopsis thaliana to high temperature and water deficit,” Acta Physiologiae Plantarum, 43, 58. Available at: https://doi.org/10.1007/s11738-021-03229-x.

Lakshmi, G. et al. (2023) “Exogenously applied plant growth regulator protects rice from heat-induced damage by modulating plant defense mechanisms,” Journal of Crop Science and Biotechnology, 26, pp. 63–75. Available at: https://doi.org/10.1007/s12892-022-00162-4.

Lamers, J., Meer van der, T. and Testerink, C. (2020) “How plants sense and respond to stressful environments,” Plant Physiology, 182, pp. 1624–1635. Available at: https://doi.org/10.1104/pp.19.01464.

Li, G. et al. (2023) “Selection and validation of reference genes in virus-infected sweet potato plants,” Genes, 14, 1477. Available at: https://doi.org/10.3390/genes14071477.

Li, S. et al. (2019) “Heat-responsive proteomics of a heat-sensitive spinach variety,” International Journal of Molecular Sciences, 20 (16), 3872. Available at: https://doi.org/10.3390/ijms20163872.

Li, S. et al. (2020) “Changes in photosynthesis and respiratory metabolism of maize seedlings growing under low-temperature stress may be regulated by arbuscular mycorrhizal fungi,” Plant Physiology and Biochemistry, 154, pp. 1–10. Available at: https://doi.org/10.1016/j.plaphy.2020.05.025.

Logan, M. (2010) Biostatistical design and analysis using R: A practical guide. Chichester: Wiley-Blackwell.

Luan, H. et al. (2018) “Elucidating the hypoxic stress response in barley (Hordeum vulgare L.) during waterlogging: A proteomics approach,” Scientific Reports, 8, 9655. Available at: https://doi.org/10.1038/s41598-018-27726-1.

Manoli, A. et al. (2012) “Evaluation of candidate reference genes for qPCR in maize,” Journal of Plant Physiology, 169, pp. 807–815. Available at: https://doi.org/10.1016/j.jplph.2012.01.019.

Mantri, N. et al. (2012) “Abiotic stress responses in plants: Present and future,” in P. Ahmad and M.N.V. Prasad (eds.) Abiotic stress responses in plants: Metabolism, productivity and sustainability. New York: Springer. Available at: https://doi.org/10.1007/978-1-4614-0634-1_1.

Mihaljević, I. et al. (2020) “Photochemical efficiency of photosystem II in two apple cultivars affected by elevated temperature and excess light in vivo,” South African Journal of Botany, 130, pp. 316–326. Available at: https://doi.org/10.1016/j.sajb.2020.01.017.

Moreira-de-Sousa, C., Souza de, R.B. and Fontanetti, C.S. (2018) “HSP70 as a biomarker: An excellent tool in environmental contamination analysis – A review,” Water Air Soil Pollution, 229, 264. Available at: https://doi.org/10.1007/s11270-018-3920-0.

Mubeen, M. et al. (2021) “Effect of plant growth promoting bacteria and drought on spring maize (Zea mays L.),” Pakistan Journal of Botany, 53, pp. 731–739. Available at: https://dx.doi.org/10.30848/PJB2021-2(38).

Mustafa, T. et al. (2021) “Exogenous application of silicon improves the performance of wheat under terminal heat stress by triggering physio-biochemical mechanisms,” Scientific Reports, 11, 23170. Available at: https://doi.org/10.1038/s41598-021-02594-4.

Netto, A.T. et al. (2005) “Photosynthetic pigments, nitrogen, chlorophyll a fluorescence and SPAD-502 readings in coffee leaves,” Scientia Horticulture, 104, pp. 199–209. Available at: https://doi.org/10.1016/j.scienta.2004.08.013.

Pan, J. et al. (2021) “Mechanisms of waterlogging tolerance in plants: Research progress and prospects,” Frontiers in Plant Science, 11, 627331. Available at: https://doi.org/10.3389/fpls.2020.627331.

Pandey, S.N. et al. (2018) “Diversity, functions, and stress responses of soil microorganisms,” in D. Egamberdieva, P. Ahmad and Q.S. Wu (eds.) Plant microbiome: Stress response. Cham: Springer, pp. 1–19.

Piršelová, B., Boleček, P. and Gálusová, T. (2016) “Effect of cadmium and arsenic on chlorophyll fluorescence of selected soybean cultivars,” Russian Journal of Plant Physiology, 63, pp. 469–473. Available at: https://doi.org/10.1134/S1021443716040129.

Qi, M. et al. (2021) “Photosynthetic resistance and resilience under drought, flooding, and rewatering in maize plants,” Photosynthetic Research, 148, pp. 1–15. Available at: https://doi.org/10.1007/s11120-021-00825-3.

R Core Team (2024) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available at: https://www.r-project.org (Accessed: June 05, 2025).

Ramazan, S. et al. (2021) “Combined gas exchange characteristics, chlorophyll fluorescence, and response curves as selection traits for temperature tolerance in maize genotypes,” Photosynthetic Research, 150, pp. 213–225. Available at: https://doi.org/10.1007/s11120-021-00829-z.

Rana, R.M. et al. (2018) “HSP70 mediated stress modulation in plants,” in A.A. Asea and P. Kaur (eds.) Heat shock proteins and stress. Cham: Springer, pp. 281–290. Available at: https://doi.org/10.1007/978-3-319-90725-3_13.

Reigosa, R.M. and Weiss, O. (2001) “Fluorescence techniques,” in R.M. Reigosa (ed.) Handbook of plant ecophysiology techniques. Dordrecht: Academic Publishers, pp. 155–171.

Rodríguez, A.A. et al. (2023) “Field and genetic evidence support the photosynthetic performance index (PIABS) as an indicator of rice grain yield,” Plant Physiology and Biochemistry, 201, 107897. Available at: https://doi.org/10.1016/j.plaphy.2023.107897.

Ruiz-Huerta, E.A. et al. (2022) “Bioaccumulation of heavy metals and As in maize (Zea mays L.) grown close to mine tailings strongly impacts plant development,” Ecotoxicology, 31, pp. 447–467. Available at: https://doi.org/10.1007/s10646-022-02522-w.

Saleem, M.H. et al. (2024) “Advances in physiochemical and molecular mechanisms of abiotic stress tolerance in plants,” Journal of Crop Health, 76, pp. 753–767. Available at: https://doi.org/10.1007/s10343-024-00993-x.

Sarkar, N.K., Kundnani, P. and Grover, A. (2013) “Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa),” Cell Stress Chaperones, 18, pp. 427–437. Available at: https://doi.org/10.1007/s12192-012-0395-6.

Scafaro, A.P. et al. (2016) “Heat tolerance in a wild Oryza species is attributed to maintenance of Rubisco activation by a thermally stable Rubisco activase ortholog,” New Phytologist, 211, pp. 899– 911. Available at: https://doi.org/10.1111/nph.13963.

Schansker, G., Tóth, S.Z. and Strasser, R.J. (2005) “Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP,” Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1706(3), pp. 250–261. Available at: https://doi.org/10.1016/j.bbabio.2004.11.006.

Schmittgen, T.D and Livak, K.J. (2008) “Analyzing real-time PCR data by the comparative CT method,” Nature Protocols, 3, pp. 1101– 1108. Available at: https://doi.org/10.1038/nprot.2008.73.

Schreiber, U., Bilger, W. and Neubauer, C. (1995) “Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis,” in E.D. Schulze and M.M. Caldwell (eds.) Ecophysiology of photosynthesis, Vol. 100. Berlin: Springer, pp. 49–70. Available at: https://doi.org/10.1007/978-3-642-79354-7_3.

Seguí-Simarro, J.M., Testillano, P.S. and Risueño, M.C. (2003) “Hsp70 and Hsp90 change their expression and subcellular localization after microspore embryogenesis induction in Brassica napus L.,” Journal of Structural Biology, 142, pp. 379–391. Available at: https://doi.org/10.1016/S1047-8477(03)00067-4.

Sena, S.J. et al. (2018) “Expansion of the dehydrin gene family in the Pinaceae is associated with considerable structural diversity and drought-responsive expression,” Tree Physiology, 38, pp. 442–456. Available at: https://doi.org/10.1093/treephys/tpx125.

Sevgi, B. and Leblebici, S. (2023) “Tuz Stresinin Bitkiler Üzerindeki Etkileri ve Geliştirilen Tolerans Mekanizmaları [Effects of salt stress on plants and developed tolerance mechanisms],” Duzce University Journal of Science and Technology, 11, pp. 1498–1516. Available at: https://doi.org/10.29130/dubited.1171221.

Sharma, A. et al. (2019) “Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress,” Molecules, 24, 2452. Available at: https://doi.org/10.3390/molecules24132452.

Shin, K.Y., Bhandari, R.S. and Lee, G.J. (2021) “Monitoring of salinity, temperature, and drought stress in grafted watermelon seedlings using chlorophyll fluorescence,” Frontiers in Plant Science, 12, 786309. Available at: https://doi.org/10.3389/fpls.2021.786309.

Song, X., Zhou, G. and He, Q. (2021) “Critical leaf water content for maize photosynthesis under drought stress and its response to rewatering,” Sustainability, 13, 7218. Available at: https://doi.org/10.3390/su13137218.

Strasser, R.J. et al. (2010) “Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis,” Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1797(6–7), pp. 1313–1326. Available at: https://doi.org/10.1016/j.bbabio.2010.03.008.

Strasser, R.J., Tsimilli-Michael, M. and Srivastava, A. (2000) “The fluorescence transient as a tool to characterize and screen photosynthetic samples,” in M. Yunus, U. Pathre and P. Mohanty (eds.) Probing photosynthesis: Mechanisms, regulation, and adaptation. London: Taylor & Francis, pp. 445–483.

Strasser, R.J., Tsimilli-Michael, M. and Srivastava, A. (2004) “Analysis of the chlorophyll a fluorescence transient,” in G.C. Papageorgiou, Govindjee (eds.) Chlorophyll a fluorescence: A signature of photosynthesis. Dordrecht: Springer, pp. 321–362. Available at: https://doi.org/10.1007/978-1-4020-3218-9_12.

Su, P.H. and Li, H.M. (2010) “Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts,” Plant Cell, 22, pp. 1516–1531. Available at: https://doi.org/10.1105/tpc.109.071415.

Sun, Z. et al. (2021) “Plant dehydrins: Expression, regulatory networks, and protective roles in plants challenged by abiotic stress,” International Journal of Molecular Science, 22, 12619. Available at: https://doi.org/10.3390/ijms222312619.

Theocharis, A., Clement, C. and Barka, E.A (2012) “Physiological and molecular changes in plants grown at low temperatures,” Planta, 235, pp. 1091–1105. Available at: https://doi.org/10.1007/s00425-012-1641-y.

Tikkanen, M., Mekala, N.R. and Aro, E.M. (2014) “Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage,” Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1837, pp. 210–215. Available at: https://doi.org/10.1016/j.bbabio.2013.10.001.

Timperio, A.M., Egidi, M.G. and Zolla, L. (2008) “Proteomics applied on plant abiotic stresses: Role of heat shock proteins (HSP),” Journal of Proteomics, 71, pp. 391–411. Available at: https://doi.org/10.1016/j.jprot.2008.07.005.

Tobiasz-Salach, R., Mazurek, M. and Jacek, B. (2023) “Physiological, biochemical, and epigenetic reaction of maize (Zea mays L.) to cultivation in conditions of varying soil salinity and foliar application of silicon,” International Journal of Molecular Sciences, 24, 1141. Available at: https://doi.org/10.3390/ijms24021141.

Tsimilli-Michael, M. (2020) “Revisiting JIP-test: An educative review on concepts, assumptions, approximations, definitions and terminology,” Photosynthetica, 58, pp. 275–292. Available at: https://doi.org/10.32615/ps.2019.150.

Wahid, A. et al. (2007) “Heat tolerance in plants: An overview,” Environmental and Experimental Botany, 61, pp. 199–223. Available at: https://doi.org/10.1016/j.envexpbot.2007.05.011.

Wang, K. et al. (2019) “The role of C2H2 zinc finger proteins in plant responses to abiotic stresses,” Physiologia Plantarum, 165, pp. 690–700. Available at: https://doi.org/10.1111/ppl.12728.

Wang, Y.-Y., Head, D.J. and Hauser, B.A. (2023) “During water stress, fertility modulated by ROS scavengers abundant in Arabidopsis pistils,” Plants, 12, 2182. Available at: https://doi.org/10.3390/plants12112182.

Yang, X. et al. (2021) “Response mechanism of plants to drought stress,” Horticulturae, 7, 50. Available at: https://doi.org/10.3390/horticulturae7030050.

Zalewski, D. (2024) RQdeltaCT: Relative quantification of gene expression using delta Ct methods. R package version 1.3.0. Available at: https://doi.org/10.32614/CRAN.package.RQdeltaCT (Accessed: April 01, 2025).

Zhang, Z. et al. (2020) “Calcium is involved in exogenous NO-induced enhancement of photosynthesis in cucumber (Cucumis sativus L.) seedlings under low temperature,” Scientia Horticulturae, 261, 108953. Available at: https://doi.org/10.1016/j.scienta.2019.108953.

Zhao, H. et al. (2019) “Effects of salt stress on chlorophyll fluorescence and the antioxidant system in Ginkgo biloba L. seedlings,” HortScience, 54(12), pp. 2125–2133. Available at: https://doi.org/10.21273/HORTSCI14432-19.

Zhou, S. et al. (2022) “Small heat shock proteins and dehydrins synergistically stabilize chloroplast proteins during salt stress,” Plant Cell Environment, 45, pp. 847–864. Available at: https://doi.org/10.1111/pce.14256.

Zivčák, M. et al. (2014) “Photosynthetic responses of sun- and shade- grown barley leaves to high light: Is the lower PSII photochemical efficiency in shade leaves associated with decreased PSII antenna size?,” Photosynthetic Research, 119, pp. 339–354. Available at: https://doi.org/10.1007/s11120-014-9969-8.