High temperatures have significant impacts on fruit tree production. Foliar spraying application of promoting agents can be a sustainable approach to managing high-temperature stress in orchards. The mechanism of certain improving agents on photosynthesis is not yet well understood, particularly in fruit trees. Photosynthesis, as a vital and very sensitive process in plants, is a pivotal component in fruit production. Therefore, in this study, we explored the potential of two different promoting agents, salicylic acid (SA) and ascorbic acid (AsA), to alleviate oxidative stress caused by high temperature in controlled conditions (37°C for 1 h) at the photosynthetic level. For studying photosynthetic responses, we used chlorophyll fluorescence measurements. According to our findings, foliar application of promoting agents effectively increased the high-temperature tolerance of apple leaves, when compared to sole heat stress treatment. Both promoting agents significantly increased photosynthetic efficiency under stress, while the maximum was observed with AsA. In general, AsA and SA applications had a positive effect on the photosynthesis of apple leaves at high temperatures.

Agricultural Institute Osijek Južno predgrađe 17 HR 31000 Osijek Croatia

Zobrazit více v PubMed

Akram N.A., Shafiq F., Ashraf M.: Ascorbic acid – a potential oxidant scavenger and its role in plant development and abiotic stress tolerance. – Front. Plant Sci. 8: 613, 2017. 10.3389/fpls.2017.00613 PubMed DOI PMC

Allahveran A., Farokhzad A., Asghari M., Sarkhosh A.: Foliar application of ascorbic and citric acids enhanced ‘Red Spur’ apple fruit quality, bioactive compounds and antioxidant activity. – Physiol. Mol. Biol. Plants 24: 433-440, 2018. 10.1007/s12298-018-0514-7 PubMed DOI PMC

Allakhverdiev S.I., Kreslavski V.D., Klimov V.V. et al.: Heat stress: an overview of molecular responses in photosynthesis. – Photosynth. Res. 9: 541-550, 2008. 10.1007/s11120-008-9331-0 PubMed DOI

Antunović Dunić J., Mlinarić S., Pavlović I. et al.: Comparative analysis of primary photosynthetic reactions assessed by OJIP kinetics in three Brassica crops after drought and recovery. – Appl. Sci. 13: 3078, 2023. 10.3390/app13053078 DOI

Bukhat S., Manzoor H., Athar HuR. et al.: Salicylic acid induced photosynthetic adaptability of Raphanus sativus to salt stress is associated with antioxidant capacity. – J. Plant Growth Regul. 39: 809-822, 2020. 10.1007/s00344-019-10024-z DOI

Chen K., Sun X., Amombo E. et al.: High correlation between thermotolerance and photosystem II activity in tall fescue. – Photosynth. Res. 122: 305-314, 2014. 10.1007/s11120-014-0035-3 PubMed DOI

Chen K., Zhang M., Zhu H. et al.: Ascorbic acid alleviates damage from heat stress in the photosystem II of tall fescue in both the photochemical and thermal phases. – Front. Plant Sci. 8: 1373, 2017. 10.3389/fpls.2017.01373 PubMed DOI PMC

Chen L.S., Cheng L.: Photosystem 2 is more tolerant to high temperature in apple (Malus domestica Borkh.) leaves than in fruit peel. – Photosynthetica 47: 112-120, 2009. 10.1007/s11099-009-0017-4 DOI

Chen S., Yang J., Zhang M. et al.: Classification and characteristics of heat tolerance in Ageratina adenophora populations using fast chlorophyll a fluorescence rise O-J-I-P. – Environ. Exp. Bot. 122: 126-140, 2016. 10.1016/j.envexpbot.2015.09.011 DOI

Chen X., Zhou Y., Cong Y. et al.: Ascorbic acid-induced photosynthetic adaptability of processing tomatoes to salt stress probed by fast OJIP fluorescence rise. – Front. Plant Sci. 12: 594400, 2021. 10.3389/fpls.2021.594400 PubMed DOI PMC

De Ronde J.A., Cress W.A., Krüger G.H.J. et al.: Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. – J. Plant Physiol. 161: 1211-1224, 2004. 10.1016/j.jplph.2004.01.014 PubMed DOI

Dimitrova S., Paunov M., Pavlova B. et al.: Photosynthetic efficiency of two Platanus orientalis L. ecotypes exposed to moderately high temperature: JIP-test analysis. – Photosynthetica 58: 657-670, 2020. 10.32615/ps.2020.012 DOI

Duan N., Bai Y., Sun H. et al.: Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. – Nat. Commun. 8: 249, 2017. 10.1038/s41467-017-00336-7 PubMed DOI PMC

Ergin S., Aydogan C., Ozturk N., Turhan E.: Effects of ascorbic acid application in strawberry plants during heat stress. – Turk. J. Agric. Nat. Sci. 2: 1486-1491, 2014. https://dergipark.org.tr/en/download/article-file/142294

Farooq A., Bukhari S.A., Akram N.A. et al.: Exogenously applied ascorbic acid-mediated changes in osmoprotection and oxidative defense system enhanced water stress tolerance in different cultivars of safflower (Carthamus tinctorious L.). – Plants-Basel 9: 104, 2020. 10.3390/plants9010104 PubMed DOI PMC

Felicetti D.A., Schrader L.E.: Changes in pigment concentrations associated with the degree of sunburn browning of ‘Fuji’ apple. – J. Am. Soc. Hortic. Sci. 133: 27-34, 2008. 10.21273/JASHS.133.1.27 DOI

Feng B., Liu P., Li G. et al.: Effect of heat stress on the photosynthetic characteristics in flag leaves at the grain-filling stage of different heat-resistant winter wheat varieties. – J. Agron. Crop Sci. 200: 143-155, 2014. 10.1111/jac.12045 DOI

Gao Y., Liu W., Wang X. et al.: Comparative phytotoxicity of usnic acid, salicylic acid, cinnamic acid and benzoic acid on photosynthetic apparatus of Chlamydomonas reinhardtii. – Plant Physiol. Biochem. 128: 1-12, 2018. 10.1016/j.plaphy.2018.04.037 PubMed DOI

Ghaffar A., Hussain N., Ajaj R.: Photosynthetic activity and metabolic profiling of bread wheat cultivars contrasting in drought tolerance. – Front. Plant Sci. 14: 1123080, 2023. 10.3389/fpls.2023.1123080 PubMed DOI PMC

Giorio P., Sellami M.H.: Polyphasic OKJIP chlorophyll a fluorescence transient in a landrace and a commercial cultivar of sweet pepper (Capsicum annuum L.) under long-term salt stress. – Plants-Basel 10: 887, 2021. 10.3390/plants10050887 PubMed DOI PMC

Haldimann P., Feller U.: Growth at moderately elevated temperature alters the physiological response of the photosynthetic apparatus to heat stress in pea (Pisum sativum L.) leaves. – Plant Cell Environ. 28: 302-317, 2005. 10.1111/j.1365-3040.2005.01289.x DOI

Huther C.M., Ramm A., Rombaldi C.V., Bacarin M.A.: Physiological response to heat stress of tomato ‘Micro-Tom’ plants expressing high and low levels of mitochondrial sHSP23.6 protein. – Plant Growth. Regul. 70: 175-185, 2013. 10.1007/s10725-013-9790-y DOI

Iqbal N., Fatma M., Gautam H. et al.: Salicylic acid increases photosynthesis of drought grown mustard plants effectively with sufficient-N via regulation of ethylene, abscisic acid, and nitrogen-use efficiency. – J. Plant Growth Regul. 41: 1966-1977, 2022. 10.1007/s00344-021-10565-2 DOI

Jahan M.S., Wang Y., Shu S. et al.: Exogenous salicylic acid increases the heat tolerance in tomato (Solanum lycopersicum L) by enhancing photosynthesis efficiency and improving antioxidant defense system through scavenging of reactive oxygen species. – Sci. Hortic.-Amsterdam 247: 421-429, 2019. 10.1016/j.scienta.2018.12.047 DOI

Janda T., Gondor O.K., Yordanova R. et al.: Salicylic acid and photosynthesis: signalling and effects. – Acta Physiol. Plant. 36: 2537-2546, 2014. 10.1007/s11738-014-1620-y DOI

Jedmowski C., Brüggemann W.: Imaging of fast chlorophyll fluorescence induction curve (OJIP) parameters, applied in a screening study with wild barley (Hordeum spontaneum) genotypes under heat stress. – J. Photoch. Photobio. B 151: 153-160, 2015. 10.1016/j.jphotobiol.2015.07.020 PubMed DOI

Jemrić T., Fruk I., Fruk M. et al.: Bitter pit in apples: pre- and postharvest factors: a review. – Span. J. Agric. Res. 14: e08R01, 2016. https://sjar.revistas.csic.es/index.php/sjar/article/view/8491

Ji W., Hong E., Chen X. et al.: Photosynthetic and physiological responses of different peony cultivars to high temperature. – Front. Plant Sci. 13: 969718, 2022a. 10.3389/fpls.2022.969718 PubMed DOI PMC

Ji W., Luo H., Song Y. et al.: Changes in photosynthetic characteristics of Paeonia suffruticosa under high temperature stress. – Agronomy 12: 1203, 2022b. 10.3390/agronomy12051203 DOI

Jiang C.D., Jiang G.M., Wang X. et al.: Enhanced photosystem 2 thermostability during leaf growth of elm (Ulmus pumila) seedlings. – Photosynthetica 44: 411-418, 2006. 10.1007/s11099-006-0044-3 DOI

Kalaji H.M., Govindjee, Bosa K. et al.: Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. – Environ. Exp. Bot. 73: 64-72, 2011. 10.1016/j.envexpbot.2010.10.009 DOI

Kamal M.A., Saleem M.F., Shahid M. et al.: Ascorbic acid triggered physiochemical transformations at different phenological stages of heat-stressed Bt cotton. – J. Agron. Crop Sci. 203: 323-331, 2017. 10.1111/jac.12211 DOI

Kazemi M., Aran M., Zamani S.: Effect of salicylic acid treatments on quality characteristics of apple fruits during storage. – Am. J. Plant Physiol. 6: 113-119, 2011. 10.3923/ajpp.2011.113.119 DOI

Khavari M., Fatahi R., Zamani Z.: Salicylic acid and kaolin effects on pomological, physiological, and phytochemical characters of hazelnut (Corylus avellana) at warm summer condition. – Sci. Rep.-UK 11: 4568, 2021. 10.1038/s41598-021-83790-0 PubMed DOI PMC

Krause G.H., Weis E.: Chlorophyll fluorescence and photosynthesis: the basics. – Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 313-349, 1991. 10.1146/annurev.pp.42.060191.001525 DOI

Lichtenthaler H.K.: Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. – Method. Enzymol. 148: 350-382, 1987. 10.1016/0076-6879(87)48036-1 DOI

Lotfi R., Pessarakli M., Gharavi-Kouchebagh P., Khoshvaghti H.: Physiological responses of Brassica napus to fulvic acid under water stress: Chlorophyll a fluorescence and antioxidant enzyme activity. – Crop J. 3: 434-439, 2015. 10.1016/j.cj.2015.05.006 DOI

Markulj Kulundžić A., Viljevac Vuletić M., Matoša Kočar M. et al.: Effect of elevated temperature and excess light on photosynthetic efficiency, pigments, and proteins in the field-grown sunflower during afternoon. – Horticulturae 8: 392, 2022. 10.3390/horticulturae8050392 DOI

Martinazzo E.G., Ramm A., Bacarin M.A.: The chlorophyll a fluorescence as an indicator of the temperature stress in the leaves of Prunus persica. – Braz. J. Plant Physiol. 24: 237-246, 2012. 10.1590/S1677-04202013005000001 DOI

Mathur S., Jajoo A., Mehta P., Bharti S..: Analysis of elevated temperature-induced inhibition of photosystem II using chlorophyll a fluorescence induction kinetics in wheat leaves (Triticum aestivum). – Plant Biol. 13: 1-6, 2011. 10.1111/j.1438-8677.2009.00319.x PubMed DOI

Mathur S., Mehta P., Jajoo A.: Effects of dual stress (high salt and high temperature) on the photochemical efficiency of wheat leaves (Triticum aestivum). – Physiol. Mol. Biol. Plants 19: 179-188, 2013. 10.1007/s12298-012-0151-5 PubMed DOI PMC

Maxwell K., Johnson G.N.: Chlorophyll fluorescence – a practical guide. – J. Exp. Bot. 51: 659-668, 2000. 10.1093/jexbot/51.345.659 PubMed DOI

Mihaljević I., Lepeduš H., Šimić D. et al.: Photochemical efficiency of photosystem II in two apple cultivars affected by elevated temperature and excess light in vivo. – S. Afr. J. Bot. 130: 316-326, 2020. 10.1016/j.sajb.2020.01.017 DOI

Mittler R.: Oxidative stress, antioxidants and stress tolerance. – Trends Plant Sci. 7: 405-410, 2002. 10.1016/s1360-1385(02)02312-9 PubMed DOI

Moustakas M., Sperdouli I., Adamakis I.-D.S. et al.: Harnessing the role of foliar applied salicylic acid in decreasing chlorophyll content to reassess photosystem II photoprotection in crop plants. – Int. J. Mol. Sci. 23: 7038, 2022. 10.3390/ijms23137038 PubMed DOI PMC

Nazar R., Iqbal N., Syeed S., Khan N.A.: Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. – J. Plant Physiol. 168: 807-815, 2011. 10.1016/j.jplph.2010.11.001 PubMed DOI

Netshimbupfe M.H., Berner J., Gouws C.: The interactive effects of drought and heat stress on photosynthetic efficiency and biochemical defense mechanisms of Amaranthus species. – Plant-Environ. Interact. 3: 212-225, 2022. 10.1002/pei3.10092 PubMed DOI PMC

Oukarroum A., El Madidi S., Strasser RJ.: Differential heat sensitivity index in barley cultivars (Hordeum vulgare L.) monitored by chlorophyll a fluorescence OKJIP. – Plant Physiol. Biochem. 105: 102-108, 2016. 10.1016/j.plaphy.2016.04.015 PubMed DOI

Sangwan S., Shameem N., Yashveer S. et al.: Role of salicylic acid in combating heat stress in plants: Insights into modulation of vital processes. – Front. Biosci. 27: 310, 2022. 10.31083/j.fbl2711310 PubMed DOI

Schrader L., Sun J., Zhang J. et al.: Heat and light-induced apple skin disorders: causes and prevention. – Acta Hortic. 772: 51-58, 2008. 10.17660/ActaHortic.2008.772.5 DOI

Shanker A.K., Amirineni S., Bhanu D. et al.: High-resolution dissection of photosystem II electron transport reveals differential response to water deficit and heat stress isolation and combination in pearl millet [Pennisetum glaucum (L.) R. Br.]. – Front. Plant Sci. 13: 892676, 2022. 10.3389/fpls.2022.892676 PubMed DOI PMC

Shin Y.K., Bhandari S.R., Jo J.S.: Effect of drought stress on chlorophyll fluorescence parameters, phytochemical contents, and antioxidant activities in lettuce seedlings. – Horticulturae 7: 238, 2021. 10.3390/horticulturae7080238 DOI

Strasser R.J., Srivastava A., Tsimilli-Michael M.: The fluorescence transient as a tool to characterize and screen photosynthetic samples. – In: Yunus M., Pathre U., Mohanty P. (ed.): Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Pp. 445-483. Taylor & Francis, London: 2000. https://www.researchgate.net/publication/252250818_The_fluorescence_transient_as_a_tool_to_characterize_and_screen_photosynthetic_samples

Strasser R.J., Tsimilli-Michael M., Qiang S., Goltsev V.: 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. – BBA-Bioenergetics 1797: 1313-1326, 2010. 10.1016/j.bbabio.2010.03.008 PubMed DOI

Sugiura T., Ogawa H., Fukuda N., Moriguchi T.: Changes in the taste and textural attributes of apples in response to climate change. – Sci. Rep.-UK 3: 2418, 2013. 10.1038/srep02418 PubMed DOI PMC

van der Westhuizen M.M., Oosterhuis D.M., Berner J.M., Boogaers N.: Chlorophyll a fluorescence as an indicator of heat stress in cotton (Gossypium hirsutum L.). – S. Afr. J. Plant Soil 37: 116-119, 2020. 10.1080/02571862.2019.1665721 DOI

Viljevac Vuletić M., Mihaljević I., Tomaš V. et al.: Physiological response to short-term heat stress in the leaves of traditional and modern plum (Prunus domestica L.) cultivars. – Horticulturae 8: 72, 2022. 10.3390/horticulturae8010072 DOI

Wahid A., Gelani S., Ashraf M., Foolad M.R.: Heat tolerance in plants: An overview. – Environ. Exp. Bot. 61: 199-223, 2007. 10.1016/j.envexpbot.2007.05.011 DOI

Wang G., Zeng F., Song P. et al.: Effects of reduced chlorophyll content on photosystem functions and photosynthetic electron transport rate in rice leaves. – J. Plant Physiol. 272: 153669, 2022. 10.1016/j.jplph.2022.153669 PubMed DOI

Wang L.-J., Fan L., Loescher W. et al.: Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves. – BMC Plant Biol. 10: 34, 2010. 10.1186/1471-2229-10-34 PubMed DOI PMC

Wang Y., Zhang H., Hou P. et al.: Foliar-applied salicylic acid alleviates heat and high light stress induced photoinhibition in wheat (Triticum aestivum) during the grain filling stage by modulating the psbA gene transcription and antioxidant defence. – Plant Growth Regul. 73: 289-297, 2014. 10.1007/s10725-014-9889-9 DOI

Wujeska-Klause A., Bossinger G., Tausz M. et al.: Seedlings of two Acacia species from contrasting habitats show different photoprotective and antioxidative responses to drought and heatwaves. – Ann. For. Sci. 72: 403-414, 2015. 10.1007/s13595-014-0438-5 DOI

Xu H., Liu G., Liu G. et al.: Comparison of investigation methods of heat injury in grapevine (Vitis) and assessment to heat tolerance in different cultivars and species. – BMC Plant Biol. 14: 156, 2014. 10.1186/1471-2229-14-156 PubMed DOI PMC

Yan K., Chen P., Shao H. et al.: Effects of short-term high temperature on photosynthesis and photosystem II performance in sorghum. – J. Agron. Crop Sci. 197: 400-408, 2011. 10.1111/j.1439-037X.2011.00469.x DOI

Yan K., Chen P., Shao H. et al.: Dissection of photosynthetic electron transport process in sweet sorghum under heat stress. – PLoS ONE 8: e62100, 2013. 10.1371/journal.pone.0062100 PubMed DOI PMC

Yang Y.-J., Tan S.-L., Sun H. et al.: Photosystem I is tolerant to fluctuating light under moderate heat stress in two orchids Dendrobium officinale and Bletilla striata. – Plant Sci. 303: 110795, 2021. 10.1016/j.plantsci.2020.110795 PubMed DOI

Yusuf M.A., Kumar D., Rajwanshi R. et al.: Overexpression of γ-tocopherol methyltransferase gene in transgenic Brassica jumcea plants alleviates abiotic stress: Physiological and chlorophyll a fluorescence measurements. – BBA-Bioenergetics 1797: 1428-1438, 2010. 10.1016/j.bbabio.2010.02.002 PubMed DOI

Zare Bavani M.R., Peyvast G., Ghasemnezhad M., Forghani A.: Assessment of salt tolerance in pepper using chlorophyll fluorescence and mineral compositions. – Agric. Conspec. Sci. 80: 153-158, 2015. https://hrcak.srce.hr/154810

Zhang Q.L., Wei Y.X., Peng C.L.: Effects of endogenous ascorbic acid on resistance to high-temperature stress in excised rice leaves. – Photosynthetica 56: 1453-1458, 2018. 10.1007/s11099-018-0836-2 DOI

Zhang Z., Lan M., Han X. et al.: Response of ornamental pepper to high-temperature stress and role of exogenous salicylic acid in mitigating high temperature. – J. Plant Growth Regul. 39: 133-146, 2020. 10.1007/s00344-019-09969-y DOI

Zong Y., Xu C., Zhou K. et al.: Effects of exogenous ascorbic acid on photosynthesis and xanthophyll cycle in alfalfa (Medicago sativa L.) under drought and heat stress. – Plant Soil Environ. 69: 487-499, 2023. 10.17221/330/2023-PSE DOI

Zushi K., Kajiwara S., Matsuzoe N.: Chlorophyll a fluorescence OJIP transient as a tool to characterize and evaluate response to heat and chilling stress in tomato leaf and fruit. – Sci. Hortic.-Amsterdam 148: 39-46, 2012. 10.1016/j.scienta.2012.09.022 DOI