Brassinosteroids and the Tolerance of Cereals to Low and High Temperature Stress: Photosynthesis and the Physicochemical Properties of Cell Membranes

Abstract

Cereals, which belong to the Poaceae family, are the most economically important group of plants. Among abiotic stresses, temperature stresses are a serious and at the same time unpredictable problem for plant production. Both frost (in the case of winter cereals) and high temperatures in summer (especially combined with a water deficit in the soil) can result in significant yield losses. Plants have developed various adaptive mechanisms that have enabled them to survive periods of extreme temperatures. The processes of acclimation to low and high temperatures are controlled, among others, by phytohormones. The current review is devoted to the role of brassinosteroids (BR) in cereal acclimation to temperature stress with special attention being paid to the impact of BR on photosynthesis and the membrane properties. In cereals, the exogenous application of BR increases frost tolerance (winter rye, winter wheat), tolerance to cold (maize) and tolerance to a high temperature (rice). Disturbances in BR biosynthesis and signaling are accompanied by a decrease in frost tolerance but unexpectedly an improvement of tolerance to high temperature (barley). BR exogenous treatment increases the efficiency of the photosynthetic light reactions under various temperature conditions (winter rye, barley, rice), but interestingly, BR mutants with disturbances in BR biosynthesis are also characterized by an increased efficiency of PSII (barley). BR regulate the sugar metabolism including an increase in the sugar content, which is of key importance for acclimation, especially to low temperatures (winter rye, barley, maize). BR either participate in the temperature-dependent regulation of fatty acid biosynthesis or control the processes that are responsible for the transport or incorporation of the fatty acids into the membranes, which influences membrane fluidity (and subsequently the tolerance to high/low temperatures) (barley). BR may be one of the players, along with gibberellins or ABA, in acquiring tolerance to temperature stress in cereals (particularly important for the acclimation of cereals to low temperature).

Keywords: acclimation; brassinosteroids; cereals; frost; hardening; high temperature.

Figure 1

Structural formulas of the selected BR: C₂₇ (28-norcastasterone, 28-norbrassinolide), C₂₈ (castasterone, brassinolide and 24-epicastasterone, 24-epibrassinolide) and C₂₉ (homocastasterone, homobrassinolide). Figure was prepared in ChemSketch program and is based on the chemical structures of BR that are available in an article of Bajguz and Tretyn [3].

Figure 2

After-frost regrowth of the winter cereals that had been pretreated with brassinosteroids (BR). (A) Winter rye plants of the cold-acclimated control after exposure to −17 °C (left) and plants that had been sprayed with BR (24-epibrassinolide) before cold acclimation and then exposed to −17 °C (right) (based on Pociecha et al. [88], photo courtesy of E. Pociecha). Winter wheat (cultivars Nutka and Smuga): control plants that had been cold acclimated and then exposed to −12 °C (B), plants that had been sprayed with BR (24-epibrassinolide) before cold acclimation and then exposed to −12 °C (C) (based on Janeczko et al. [89]).

Figure 3

Relative percentage changes in the homocastasterone and castasterone content in the barley plants that had been acclimated at 5 °C (A,C) and 27 °C (B,D) relative to plants that had been acclimated at 20 °C. The results that were obtained for the plants that had been grown at 20 °C were considered to be 100% and are indicated by the horizontal black line. Original data of BR accumulation are available in [13]. Bowman—a reference cultivar for two NILs: BW084—plants with disturbances in the early stage of the BR biosynthetic pathway and BW312—plants with a BRI1 receptor defect. Delisa—reference cultivar for the 522DK mutant (plants with disturbances in the late stage of the BR biosynthesis pathway).

Figure 4

Dependence of the order parameter S of the model membranes that had been prepared from egg yolk lecithin (EYL) with incorporated spin labels SASL-5 (A) or SASL-16 (B) and BR (BL—brassinolide; CS—castasterone at sample concentrations corresponding to their natural concentrations in chloroplasts) on the measurement temperature of the spectra using the EPR method. (C) Model of the prepared model membrane. The liposomes were prepared according to the modified method described earlier in work Sadura [135]. Briefly, spin labels (SASL-5 or SASL-16) (0.1 mM) and BR (BL or CS) (at a certain concentration) were added to EYL (10 mM). Next, it was shaken on a vortex and centrifuged and the methanol (in which all ingredients were suspended) was evaporated under N₂ in order to obtain a film on the test tube walls. After that, a CIB buffer (pH 7.5) (described in Sadura et al. [37]) was added to the sample and it was shaken for one minute on a vortex. Next, the sample was placed in a capillary, and the EPR spectra were measured in a temperature range of 0 °C to 40 °C at intervals of 5 °C (the process of the measurements is described in Sadura et al. [37]). The presented dependence enabled a conclusion to be drawn about the molecular dynamics of the membranes. Order parameter S was calculated according to the equations presented in the work of Sadura et al. [37]. The graphs show the mean values of two measurements ± SD.