The importance of high temperature as an environmental factor is growing in proportion to deepening global climate change. The study aims to evaluate the effects of long-term acclimation of plants to elevated temperature on the tolerance of their photosynthetic apparatus to heat stress. Three wheat (Triticum sp. L.) genotypes differing in leaf and photosynthetic traits were analyzed: Thesee, Roter Samtiger Kolbenweizen, and ANK 32A. The pot experiment was established in natural conditions outdoors (non-acclimated variant), from which a part of the plants was placed in foil tunnel with elevated temperature for 14 days (high temperature-acclimated variant). A severe heat stress screening experiment was induced by an exposition of the plans in a growth chamber with artificial light and air temperature up to 45 °C for ~12 h before the measurements. The measurements of leaf photosynthetic CO2 assimilation, stomatal conductance, and rapid kinetics of chlorophyll a fluorescence was performed. The results confirmed that a high temperature drastically reduced the photosynthetic assimilation rate caused by the non-stomatal (biochemical) limitation of photosynthetic processes. On the other hand, the chlorophyll fluorescence indicated only a moderate level of decrease of quantum efficiency of photosystem (PS) II (Fv/Fm parameter), indicating mostly reversible heat stress effects. The heat stress led to a decrease in the number of active PS II reaction centers (RC/ABS) and overall activity o PSII (PIabs) in all genotypes, whereas the PS I (parameter ψREo) was negatively influenced by heat stress in the non-acclimated variant only. Our results showed that the genotypes differ in acclimation capacity to heat stress, and rapid noninvasive techniques may help screen the stress effects and identify more tolerant crop genotypes. The acclimation was demonstrated more at the PS I level, which may be associated with the upregulation of alternative photosynthetic electron transport pathways with clearly protective functions.

Department of Agriculture Food and Environment University of Pisa 56124 Pisa Italy

Department of Botany and Plant Physiology Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamycka 129 165 00 Prague Czech Republic

Department of Plant Physiology Faculty of Agrobiology and Food Resources Slovak University of Agriculture Trieda A Hlinku 2 949 76 Nitra Slovakia

Laboratory of Plant Cytophysiology Department of Environmental and Prevention Sciences University of Ferrara Corso Ercole 1 d'Este 32 44100 Ferrara Italy

State Key Laboratory of Crop Biology College of Life Science Shandong Agricultural University Taian 271018 China

Zobrazit více v PubMed

Duc N.H., Csintalan Z., Posta K. Arbuscular mycorrhizal fungi mitigate negative effects of combined drought and heat stress on tomato plants. Plant Physiol. Biochem. 2018;132:297–307. doi: 10.1016/j.plaphy.2018.09.011. PubMed DOI

Tarvainen L., Wittemann M., Mujawamariya M., Manishimwe A., Zibera E., Ntirugulirwa B., Ract C., Manzi O.J.L., Andersson M.X., Spetea C., et al. Handling the heat-photosynthetic thermal stress in tropical trees. New Phytol. 2022;23:236–250. doi: 10.1111/nph.17809. PubMed DOI

Ainsworth E.A., Ort D.R. How do we improve crop production in a warming world? Plant Biol. 2010;154:526–530. doi: 10.1104/pp.110.161349. PubMed DOI PMC

Hussain S., Ulhassan Z., Brestic M., Zivcak M., Zhou W., Allakhverdiev S.I., Liu W. Photosynthesis research under climate change. Photosynth. Res. 2021;150:5–19. doi: 10.1007/s11120-021-00861-z. PubMed DOI

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

Niinemets Ü. When leaves go over the thermal edge. Plant Cell Environ. 2018;41:1247–1250. doi: 10.1111/pce.13184. PubMed DOI

Shanmugam S., Kjaer K.H., Ottosen C.O., Rosenqvist E., Kumari Sharma D., Wollenweber B. The Alleviating Effect of Elevated CO2 on Heat Stress Susceptibility of Two Wheat (Triticum aestivum L.) Cultivars. J. Agron. Crop Sci. 2013;199:340–350. doi: 10.1111/jac.12023. DOI

Fischer R.A. Wheat physiology: A review of recent developments. Crop Pasture Sci. 2011;62:95–114. doi: 10.1071/CP10344. DOI

Howarth C.J. Genetic improvements of tolerance to high temperature. In: Ashraf M., Harris P., editors. Abiotic Stresses. CRC Press; Boca Raton, FL, USA: 2005. pp. 299–322.

Schoeffl F., Prandl R., Reindl A. Molecular responses to heat stress. In: Shinozaki K., Yamaguchi-Shinozaki K., editors. Molecular Responses to Cold, Drought, Heat and Salt Stress in Higher Plants. R.G. Landes Co.; Austin, TX, USA: 1999. pp. 81–98.

Berry J., Bjorkman O. Photosynthetic response and adaptation to temperature in higher plants. Annu. Rev. Plant Physiol. 1980;31:491–543. doi: 10.1146/annurev.pp.31.060180.002423. DOI

Hueve K., Bichele I., Rasulov B., Niinemets Ü.L.O. When it is too hot for photosynthesis: Heat-induced instability of photosynthesis in relation to respiratory burst, cell permeability changes and H2O2 formation. Plant Cell Environ. 2011;34:113–126. doi: 10.1111/j.1365-3040.2010.02229.x. PubMed DOI

Havaux M., Tardy F. Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: Possible involvement of xanthophyll-cycle pigments. Planta. 1996;198:324–333. doi: 10.1007/BF00620047. DOI

Camejo D., Rodríguez P., Morales M.A., Dell’Amico J.M., Torrecillas A., Alarcón J.J. High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. J. Plant Physiol. 2005;162:281–289. doi: 10.1016/j.jplph.2004.07.014. PubMed DOI

Yamane Y., Kashino Y., Koike H., Satoh K. Effects of high temperatures on the photosynthetic systems in spinach: Oxygen-evolving activities, fluorescence characteristics and the denaturation process. Photosynth. Res. 1998;57:51–59. doi: 10.1023/A:1006019102619. DOI

Nishiyama Y., Murata N. Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. Appl. Microbiol. Biotechnol. 2014;98:8777–8796. doi: 10.1007/s00253-014-6020-0. PubMed DOI

Brestic M., Zivcak M., Kalaji H.M., Carpentier R., Allakhverdiev S.I. Photosystem II thermostability in situ: Environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiol. Biochem. 2012;57:93–105. doi: 10.1016/j.plaphy.2012.05.012. PubMed DOI

Zivcak M., Brestic M., Balatova Z., Drevenakova P., Olsovska K., Kalaji H.M., Allakhverdiev S.I. Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth. Res. 2013;117:529–546. doi: 10.1007/s11120-013-9885-3. PubMed DOI

Boucher N., Carpentier R. Heat-stress stimulation of oxygen uptake by photosystem I involves the reduction of superoxide radicals by specific electron donors. Photosynth. Res. 1993;35:213–218. doi: 10.1007/BF00016552. PubMed DOI

Zhang R., Sharkey T.D. Photosynthetic electron transport and proton flux under moderate heat stress. Photosynth. Res. 2009;100:29–43. doi: 10.1007/s11120-009-9420-8. PubMed DOI

Fauset S., Oliveira L., Buckeridge M.S., Foyer C.H., Galbraith D., Tiwari R., Gloor M. Contrasting responses of stomatal conductance and photosynthetic capacity to warming and elevated CO2 in the tropical tree species Alchornea glandulosa under heatwave conditions. Environ. Exp. Bot. 2019;158:28–39. doi: 10.1016/j.envexpbot.2018.10.030. DOI

Slot M., Winter K. Photosynthetic acclimation to warming in tropical forest tree seedlings. J. Exp. Bot. 2017;68:2275–2284. doi: 10.1093/jxb/erx071. PubMed DOI PMC

Crafts-Brandner S.J., Salvucci M.E. Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc. Natl. Acad. Sci. USA. 2000;97:13430–13435. doi: 10.1073/pnas.230451497. PubMed DOI PMC

Morales D., Rodríguez P., Dell’Amico J., Nicolas E., Torrecillas A., Sánchez-Blanco M.J. High-temperature preconditioning and thermal shock imposition affects water relations, gas exchange and root hydraulic conductivity in tomato. Biol. Plant. 2003;47:203–208. doi: 10.1023/B:BIOP.0000022252.70836.fc. DOI

Yamori W., Hikosaka K., Way D.A. Temperature response of photosynthesis in C3, C4, and CAM plants: Temperature acclimation and temperature adaptation. Photosynth. Res. 2014;119:101–117. doi: 10.1007/s11120-013-9874-6. PubMed DOI

Yamasaki T., Yamakawa T., Yamane Y., Koike H., Satoh K., Katoh S. Temperature acclimation of photosynthesis and related changes in photosystem II electron transport in winter wheat. Plant Physiol. 2002;128:1087–1097. doi: 10.1104/pp.010919. PubMed DOI PMC

Posch B.C., Kariyawasam B.C., Bramley H., Coast O., Richards R.A., Reynolds M.P., Atkin O.K. Exploring high temperature responses of photosynthesis and respiration to improve heat tolerance in wheat. J. Exp. Bot. 2019;70:5051–5069. doi: 10.1093/jxb/erz257. PubMed DOI

Brestic M., Zivcak M., Hauptvogel P., Misheva S., Kocheva K., Yang X., Allakhverdiev S.I. Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions. Photosynth. Res. 2018;136:245–255. doi: 10.1007/s11120-018-0486-z. PubMed DOI

Botyanszka L., Zivcak M., Chovancek E., Sytar O., Barek V., Hauptvogel P., Brestic M. Chlorophyll fluorescence kinetics may be useful to identify early drought and irrigation effects on photosynthetic apparatus in field-grown wheat. Agronomy. 2020;10:1275. doi: 10.3390/agronomy10091275. DOI

Chovancek E., Zivcak M., Brestic M., Hussain S., Allakhverdiev S.I. The different patterns of post-heat stress responses in wheat genotypes: The role of the transthylakoid proton gradient in efficient recovery of leaf photosynthetic capacity. Photosynth. Res. 2021;150:179–193. doi: 10.1007/s11120-020-00812-0. PubMed 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., editors. Probing Photosynthesis: Mechanism, Regulation and Adaptation. Taylor and Francis; London, UK: 2000. pp. 443–480.

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. Biochim. Biophys. Acta Bioenerg. 2010;1797:1313–1326. doi: 10.1016/j.bbabio.2010.03.008. PubMed DOI

Stirbet A. On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: Basics and applications of the OJIP fluorescence transient. J. Photochem. Photobiol. B Biol. 2011;104:236–257. doi: 10.1016/j.jphotobiol.2010.12.010. PubMed DOI

Klughammer C., Schreiber U. Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. PAM Appl. Notes. 2008;1:201–247.

Chovancek E., Zivcak M., Botyanszka L., Hauptvogel P., Yang X., Misheva S., Brestic M. Transient heat waves may affect the photosynthetic capacity of susceptible wheat genotypes due to insufficient photosystem I photoprotection. Plants. 2019;8:282. doi: 10.3390/plants8080282. PubMed DOI PMC

Gupta N.K., Agarwal S., Agarwal V.P. Effect of short-term heat stress on growth, physiology and antioxidative defence system in wheat seedlings. Acta Physiol. Plant. 2013;35:1837–1842. doi: 10.1007/s11738-013-1221-1. DOI

Mott K.A., Peak D. Stomatal responses to humidity and temperature in darkness. Plant Cell Environ. 2010;33:1084–1090. doi: 10.1111/j.1365-3040.2010.02129.x. PubMed DOI

Lahr E.C., Schade G.W., Crossett C.C., Watson M.R. Photosynthesis and isoprene emission from trees along an urban–rural gradient in Texas. Glob. Chang. Biol. Bioenerg. 2015;21:4221–4236. doi: 10.1111/gcb.13010. PubMed DOI

von Caemmerer S., Evans J.R. Temperature responses of mesophyll conductance differ greatly between species. Plant Cell Environ. 2015;38:629–637. doi: 10.1111/pce.12449. PubMed DOI

Reynolds M.P., Nagarajan S., Razzaue M.A., Ageeb O.A.A. Wheat Special Report No. 42. CIMMYT; El Batán, Mexico: 1997. Using Canopy Temperature Depression to Select for Yield Potential of Wheat in Heat-Stressed Environmental.

Fischer R.A., Rees D., Sayre K.D., Lu Z.M., Condon A.G., Saavedra A.L. Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies. Crop Sci. 1998;38:1467–1475. doi: 10.2135/cropsci1998.0011183X003800060011x. DOI

Sinsawat V., Leipner J., Stamp P., Fracheboud Y. Effect of heat stress on the photosynthetic apparatus in maize (Zea mays L.) grown at control or high temperature. Environ. Exp. Bot. 2004;52:123–129. doi: 10.1016/j.envexpbot.2004.01.010. DOI

Enami I., Kitamura M., Tomo T., Isokawa Y., Ohta H., Katoh S. Is the primary cause of thermal inactivation of oxygen evolution in spinach PS II membranes release of the extrinsic 33 kDa protein or of Mn? Biochim. Biophys. Acta BBA Bioenerg. 1994;1186:52–58. doi: 10.1016/0005-2728(94)90134-1. DOI

Force L., Critchley C., Van Rensen J.J.S. New fluorescence parameters formonitoring photosynthesis in plants. Photosynth. Res. 2003;78:17–33. doi: 10.1023/A:1026012116709. PubMed DOI

Tsimilli-Michael M. Revisiting JIP-test: An educative review on concepts, assumptions, approximations, definitions and terminology. Photosynthetica. 2020;58:275–292. doi: 10.32615/ps.2019.150. DOI

Strasser R.J., Srivatsava A., Govindjee Polyphasic chlorophyll a fluorescence transients in plants and cyanobacteria. Photochem. Photobiol. 1995;61:32–42. doi: 10.1111/j.1751-1097.1995.tb09240.x. DOI

Redillas M.C.F.R., Jeong J.S., Strasser R.J., Kim Y.S., Kim J.K. JIP analysis on rice (Oryza sativa cv Nipponbare) grown under limited nitrogen conditions. J. Korean Soc. Appl. Biol. Chem. 2011;54:827–832. doi: 10.1007/BF03253169. DOI

Stirbet A., Lazár D., Kromdijk J. Chlorophyll a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica. 2018;56:86–104. doi: 10.1007/s11099-018-0770-3. DOI

Zivcak M., Olsovska K., Slamka P., Galambosova J., Rataj V., Shao H.B., Kalaji M.H., Brestic M. Measurements of chlorophyll fluorescence in different leaf positions may detect nitrogen deficiency in wheat. Zemdirbyste. 2014;101:437–444. doi: 10.13080/z-a.2014.101.056. DOI

Mishra R.K., Singhal G.S. Function of photosynthetic apparatus of intact wheat leaves under high light and heat-stress and its relationship with peroxidation of thylakoid lipids. Plant Physiol. 1992;98:1–6. doi: 10.1104/pp.98.1.1. PubMed DOI PMC

Bukhov N.G., Sabat S.C., Mohanty P. Analysis of chlorophyll a fluorescence changes in weak light in heat treated Amaranthus chloroplasts. Photosynth. Res. 1990;23:81–87. doi: 10.1007/BF00030066. PubMed DOI

Murchie E.H., Niyogi K.K. Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol. 2011;155:86–92. doi: 10.1104/pp.110.168831. PubMed DOI PMC

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

Strauss A.J., Krüger G.H.J., Strasser R.J., Heerden P.D.R.V. Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient O-J-I-P. Environ. Exp. Bot. 2006;56:147–157. doi: 10.1016/j.envexpbot.2005.01.011. DOI

Yan K., Chen P., Shao H., Shao C., Zhao S., Brestic M. Dissection of photosynthetic electron transport process in sweet sorghum under heat stress. PLoS ONE. 2013;8:e62100. doi: 10.1371/journal.pone.0062100. PubMed DOI PMC

Zivcak M., Brestic M., Kunderlikova K., Olsovska K., Allakhverdiev S.I. Effect of photosystem I inactivation on chlorophyll a fluorescence induction in wheat leaves: Does activity of photosystem I play any role in OJIP rise? J. Photochem. Photobiol. B Biol. 2015;152:318–324. doi: 10.1016/j.jphotobiol.2015.08.024. PubMed DOI

Pšidová E., Živčák M., Stojnić S., Orlović S., Gömöry D., Kučerová J., Kalaji H.M. Altitude of origin influences the responses of PSII photochemistry to heat waves in European beech (Fagus sylvatica L.) Environ. Exp. Bot. 2018;152:97–106. doi: 10.1016/j.envexpbot.2017.12.001. DOI

Zivcak M., Brestic M., Botyanszka L., Chen Y.E., Allakhverdiev S.I. Phenotyping of isogenic chlorophyll-less bread and durum wheat mutant lines in relation to photoprotection and photosynthetic capacity. Photosynth. Res. 2019;139:239–251. PubMed

Brestic M., Zivcak M., Kunderlikova K., Allakhverdiev S.I. High temperature specifically affects the photoprotective responses of chlorophyll b-deficient wheat mutant lines. Photosynth. Res. 2016;130:251–266. doi: 10.1007/s11120-016-0249-7. PubMed DOI

Ferroni L., Živčak M., Sytar O., Kovár M., Watanabe N., Pancaldi S., Brestič M. Chlorophyll-depleted wheat mutants are disturbed in photosynthetic electron flow regulation but can retain an acclimation ability to a fluctuating light regime. Environ. Exp. Bot. 2020;178:104156. doi: 10.1016/j.envexpbot.2020.104156. DOI

Brestic M., Zivcak M., Kunderlikova K., Sytar O., Shao H., Kalaji H.M., Allakhverdiev S.I. Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. Photosynth. Res. 2015;125:151–166. doi: 10.1007/s11120-015-0093-1. PubMed DOI

Tan S.L., Yang Y.J., Liu T., Zhang S.B., Huang W. Responses of photosystem I compared with photosystem II to combination of heat stress and fluctuating light in tobacco leaves. Plant Sci. 2020;292:110371. doi: 10.1016/j.plantsci.2019.110371. PubMed DOI

Allakhverdiev S.I., Kreslavski V.D., Klimov V.V., Los D.A., Carpentier R., Mohanty P. Heat stress, an overview of molecular responses in photosynthesis. Photosynth. Res. 2008;98:541–550. doi: 10.1007/s11120-008-9331-0. PubMed DOI

Foyer C.H., Neukermans J., Queval G., Noctor G., Harbinson J. Photosynthetic control of electron transport and the regulation of gene expression. J. Exp. Bot. 2012;63:1637–1661. doi: 10.1093/jxb/ers013. PubMed DOI

Wang Q.L., Chen J.H., He N.Y., Guo F.Q. Metabolic reprogramming in chloroplasts under heat stress in plants. Int. J. Mol. Sci. 2018;19:849. doi: 10.3390/ijms19030849. PubMed DOI PMC