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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

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Abstract

The frequency and severity of heat waves are expected to increase in the near future, with a significant impact on physiological functions and yield of crop plants. In this study, we assessed the residual post-heat stress effects on photosynthetic responses of six diverse winter wheat (Triticum sp.) genotypes, differing in country of origin, taxonomy and ploidy (tetraploids vs. hexaploids). After 5 days of elevated temperatures (up to 38 °C), the photosynthetic parameters recorded on the first day of recovery (R1) as well as after the next 4–5 days of the recovery (R2) were compared to those of the control plants (C) grown under moderate temperatures. Based on the values of CO2 assimilation rate (A) and the maximum rates of carboxylation (VCmax) in R1, we identified that the hexaploid (HEX) and tetraploid (TET) species clearly differed in the strength of their response to heat stress. Next, the analyses of gas exchange, simultaneous measurements of PSI and PSII photochemistry and the measurements of electrochromic bandshift (ECS) have consistently shown that photosynthetic and photoprotective functions in leaves of TET genotypes were almost fully recovered in R2, whereas the recovery of photosynthetic and photoprotective functions in the HEX group in R2 was still rather low. A poor recovery was associated with an overly reduced acceptor side of photosystem I as well as high values of the electric membrane potential (Δψ component of the proton motive force, pmf) in the chloroplast. On the other hand, a good recovery of photosynthetic capacity and photoprotective functions was clearly associated with an enhanced ΔpH component of the pmf, thus demonstrating a key role of efficient regulation of proton transport to ensure buildup of the transthylakoid proton gradient needed for photosynthesis restoration after high-temperature episodes.

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Acknowledgments

This work was supported by the Ministry of Education, Science, Research and Sport of the Slovak Republic under the projects VEGA-1-0589-19 and VEGA 1-0683-20 and the Slovak Research and Development Agency project APVV-18-465. This work was also supported by the project OPVaI-VA/DP/2018/No. 313011T813. SIA was supported by the foundation of "systems of natural and artificial photosynthesis" (FEES-2021-0012).

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Correspondence to Marek Zivcak or Suleyman I. Allakhverdiev.

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11120_2020_812_MOESM1_ESM.tif

Suppl. Fig. 1 Representative A/Ci curves (net photosynthesis measured at different intercellular CO2 concentrations) of one of the hexaploid (HEX) and tetraploid (TET) bread wheat genotypes in controls, R1, and R2 variants. Points represent individual measurements; other data (see legend) were calculated by ACi Curve Fitting tool (v.10.0) acquired from www.landflux.org, following Ethier and Livingston (2004) (TIF 1132 kb)

Suppl. Fig. 2. Example of deconvolution of ECSt signal using the subsequent records at 520 and 546 nm (TIF 514 kb)

11120_2020_812_MOESM3_ESM.tif

Suppl. Fig. 3 Comparing the slope of change in values of parameters, i.e., the difference between controls (Control) and plants in the early post-heat stress recovery phase (R1). The maximum carboxylation rate, VCmax (A, B), and the maximum electron transport rate, Jmax (C, D), are presented. Three varieties of wheat belonging to the hexaploid (HEX) group are represented by the solid lines (A, C): Thesee (blue), SLO-16/26 (red), GRC 867 (green), whereas the three varieties belonging to the tetraploid group (TET; B, D) are indicated by the dashed lines: AZESVK2009-97 (blue), Unmedpur Mummy (red), Dušan (green) (TIF 762 kb)

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Chovancek, E., Zivcak, M., Brestic, M. et al. 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 150, 179–193 (2021). https://doi.org/10.1007/s11120-020-00812-0

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