INTRODUCTION

Photosynthetic organisms of the oxygenic type (plants, algae, and cyanobacteria) contain pigment–protein complexes of two types, photosystem 1 (PS1) and photosystem 2 (PS2), which absorb light and provide electron transfer from water oxidized in PS2 to NADP+, the terminal electron acceptor in PS1. Electron transfer along the electron transport chain (ETC) occurs with the participation of the cytochrome b6f complex and mobile electron carriers, plastoquinone and plastocyanin [1–6]. In plants, ETC carriers are embedded into the thylakoid membranes of chloroplasts. The functioning of the ETC leads to the generation of a trans-thylakoid difference in the electrochemical potentials of hydrogen ions \(\left( {\Delta {{{{\mu }}}_{{{{{\text{H}}}^{{\text{ + }}}}}}}} \right)\), which is an energy source for the operation of ATP synthase [7–9]. ATP and NADPH are macroergic products of the “light” stages of photosynthesis, used in Calvin–Benson cycle reactions for CO2 fixation and carbohydrate synthesis [10].

The structural organization of the photosynthetic apparatus (PSA) of plants is well studied. Currently, one of the main tasks of biophysics and biochemistry of photosynthesis is to elucidate the mechanisms of regulation of electron transport in chloroplasts. In natural conditions, the intensity and spectral composition of light change during the day and depend on weather conditions. Shortage of light reduces the productivity of photosynthesis. An excess of light can lead to destructive processes, for example, it may cause oxidative stress and impairment of plant PSA [11, 12]. In the course of biological evolution, photosynthetic organisms have developed mechanisms to optimize bioenergetic processes under varying external conditions (lighting [13] and temperature [14–17]). These mechanisms provide “fast” (seconds–minutes) and “long-term” (hours–days) regulation of photosynthesis. Fast regulation processes are carried out due to feedbacks that affect: (1) activation/deactivation of CBC reactions [18, 19], (2) pH-dependent regulation of ETC operation [20–23], (3) redistribution of absorbed light energy between PS1 and PS2 [24], and (4) structural and functional rearrangements of PSA in membranes [25–29]. The long-term regulatory mechanisms are associated with the synthesis or degradation of those components of PSA (including pigment–protein complexes) that affect the architecture and functional properties of chloroplasts. The ability of plants to adapt to changing environmental conditions is determined by the type of plants [30].

In the context of the problem of the mechanisms of acclimation of plants to living conditions, a comparative study of closely related plant species belonging to “contrasting” species (for example, plant species of the same genus adapted to grow in shady conditions or under intense lighting) is of interest. Previously, we studied photosynthetic parameters of two species of Tradescantia, the shade-tolerant species T. fluminensis (an endemic species growing in the humid tropical forests of southeastern Brazil) and the light loving species T. sillamontana [31–37], whose historical homeland is the semi-desert regions of Mexico and Peru [38]. Another example of this kind of research is a comparative study of the properties of PSA of two species of Cucumis plants growing in areas with hot and temperate climates, namely, C. melo (melon) and C. sativus (cucumber). The properties of chloroplast membranes isolated from melon and cucumber seedlings grown under the same experimental conditions were previously studied with the help of lipid-soluble spin probes [39]. At the same time, however, it turned out that thermally induced structural transitions in the thylakoid membranes of melon chloroplasts occurred at higher temperatures (≥35°C) than in cucumber chloroplasts (~20–25°C). Obviously, this observation demonstrated that the melon (C. melo) has adapted to the growth at relatively high temperatures characteristic of the hot climate in the areas of origin of this species.

This paper presents the results of a comparative study of the dynamics of acclimation of leaves of two “contrasting” species of Tradescantia (T. fluminensis and T. sillamontana) that occurred during long-term (months) cultivation of plants at high or low light intensity. PS2 is the most vulnerable pigment–protein complex of PSA of plants, damaged by light stress or temperature increase [40–44]. To determine the functional parameters reflecting the activity of PS2 in chloroplasts in situ (plant leaves), we studied the induction of chlorophyll a (Chl a) fluorescence emitted mainly by the pigments of the PS2 light harvesting antenna [45–48]. The contribution of non-photochemical quenching (NPQ) of the fluorescence of Chl a, reflecting the effectiveness of protective mechanisms caused by increased dissipation of excess energy in the light harvesting antenna of PS2, was also evaluated [42, 49–53]. Using the fluorescence analysis, we studied the changes in the efficiency of PS2 and NPQ generation during a long (several months) acclimation of T. fluminensis and T. sillamontana to light of high or low intensity. In addition, we investigated the functioning of PS1 by recording the redox transformations of the P700 photoreaction centers (the primary electron donor in PS1) by electron paramagnetic resonance. Our studies have shown that with an increase in the duration of acclimation of shade-tolerant T. fluminensis plants they obtained an enhanced protective reaction, manifested in the generation of NPQ already at moderate light fluxes (~200 µmol photons m–2 s–1). As a result of prolonged acclimation (more than 2 months) to high-intensity light (≥ 500 µmol photons m–2 s–1) chloroplasts of T. fluminensis lost photochemical activity faster, which was not observed for the light loving species T. sillamontana. Attenuation of photochemical activity of PSA in T. fluminensis was reversible, that is, after returning to the light of moderate intensity, their photochemical activity was restored to the level characteristic of plants acclimated to moderate light.

MATERIALS AND METHODS

Plants. The objects of the study were the leaves of the Tradescantia species T. fluminensis and T. sillamontana, obtained from the Main Botanical Garden of the Russian Academy of Sciences. The plants were grown in soil culture at room temperature (24–26°C) and relative humidity of 40–60%. Pots with plants were placed in a dark chamber, inside which there were two illuminated compartments, differing in light intensity. The light source was the lamp USS 90 highway Sh (TH FOCUS LLC, Russia), equipped with white LEDs with a color temperature of 5000 K (Nichia, Japan). The spectral composition of light produced by this lamp included the components of blue, red and far-red light necessary for the normal growth and development of plants. The intensity of illumination was measured using a Li250A quantum meter (LiCOR Biosciences, USA). The duration of the light period in the daytime was 14 h, the light fluxes were equal to 800–1000 µmol photons m–2 s–1 (“strong” light, SL) or 50–125 µmol photons m–2 s–1 (“moderate” light, ML). To measure the photosynthetic parameters of the leaves, a second or third mature leaf located in the upper part of the shoot was used. When the characteristics of the leaf were measured by biophysical methods (fluorescence analysis and EPR), the sample was illuminated from the abaxial (dorsal) side of the leaf facing the upper epidermis. Several series of long-term acclimation experiments were conducted for various plantings in the spring–summer–autumn seasons of 2015–2022. The general patterns of the dynamics of changes in the biophysical parameters of the leaves of two species of Tradescantia, T. fluminenesis and T. sillamontana, studied in different seasons, were the same. In this paper, to illustrate these patterns, we present the results of studies conducted in 2019–2021.

Fluorescence measurements and NPQ determination. The fluorescence of Chl a was measured in vivo using a PAM FluorPen FP100 fluorimeter (Photon Systems Instruments, Czech Republic), as described earlier [32–37, 54]. The spectra of continuous light (“actinic” light) and weak pulses of measuring light exciting the fluorescence of Chl a had a maximum at 475 nm and a half-width of the spectral band Δλ1/2 = 25 nm. Before starting the measurements, the leaf was pre-illuminated with actinic light for 1 min (to standardize the experimental conditions), and then kept in the darkness for 10 min. The parameters of the fluorescence induction curves of Chl a and non-photochemical fluorescence quenching were determined according to traditional protocols [46–48].

The characteristic kinetic curves of fast induction of fluorescence (FIF) of Chl a in leaves in two plant species (T. fluminensis and T. sillamontana) that grew for 2 months under strong (SL) or moderate (ML) light are shown in Fig. 1. The kinetic curves of FIF show how the level of fluorescence changed during the action of the saturating pulse of light with a 2-s duration (light flux of 3000 µmol photons m–2 s–1). All these curves have characteristic features (kinks or local extremes), indicated by the symbols O, J, I and P. Parameter F0 is the initial fluorescence level of Chl a in leaves adapted to darkness. Fm is the maximum level of fluorescence measured in response to the action of a saturating pulse of light. The variable fluorescence parameter (ratio Fv/Fm = (Fm − F0)/Fm) is a measure of the maximum photochemical activity of PS2 (relative quantum yield) in leaves adapted to darkness [46–48].

Fig. 1.
figure 1

Kinetics of fast induction of fluorescence (FIF) of chlorophyll a in the leaves of T. fluminensis (a) and T. sillamontana (b) grown for 2 months under strong (SL) and moderate (ML) illumination. The measurements were carried out in accordance with the protocol described in the Materials and Methods section. The beginning of the measurements was preceded by the adaptation of the samples to darkness for 10 min. All FIF curves were normalized to the maximum intensity of fluorescence Fm.

Full size image

Figure 2 shows the typical kinetics of slow induction of fluorescence (SIF) of Chl a caused by the action of continuous light (often called “actinic” light in the literature) and short (1 s) flashes of light (λmax = 475 nm) of high intensity (3000 µmol photons m–2 s–1). The values of Fm and \(F_{{\text{m}}}^{'}\) are the fluorescence levels measured during the action of intense flashes on a sample of a leaf adapted to darkness (Fm) or during its illumination with actinic light \(\left( {F_{{\text{m}}}^{'}} \right)\). F(t) is the fluorescence intensity measured immediately before the intense flash was applied. The parameters ФPSII = 1 –F(t)/\(F_{{\text{m}}}^{'}\) and qNPQ = Fm0/\(F_{{\text{m}}}^{'}\) – 1 characterize the so-called operational efficiency of the photochemical centers of PS2 (ФPSII) and the NPQ coefficient (qNPQ), respectively [46–48].

Fig. 2.
figure 2

Kinetics of chlorophyll a fluorescence induction in T. fluminensis leaves grown under “strong” illumination of plants. The measurements were carried out in accordance with the protocol described in the section “Materials and methods”. Zigzag arrows show the moments of applying short saturating flashes of light. Vertical arrow shows the moment of switching on the continuous (actinic) light. The kinetic curve was normalized by the Fm value determined by the fluorescence level for the first saturating flash, applied after the leaf adapted to darkness for 10 min. FT is a stationary fluorescence level, which is established after a long (~10 min) illumination of leaves with actinic light intensity of 800 µmol photons m–2 s–1.

Full size image

Electron paramagnetic resonance (EPR). The characteristic EPR signal from oxidized \({\text{P}}_{{700}}^{ + }\) centers allows monitoring electron transport in chloroplasts in situ [54, 55]. A sample (a freshly cut piece of leaf of 4 × 25 mm) was fixed in a well-ventilated holder and placed in a rectangular resonator of a E-4 EPR spectrometer (Varian, USA). The power of the microwave radiation was 10 mW, the amplitude of the high frequency modulation of magnetic field was equal to 0.4 mT. The samples were illuminated with white light (WL, 320 W m–2), effectively exciting both photosystems, or with far-red light (FRL, λmax = 707 nm, 8 W m–2), exciting predominantly PS1. The kinetics of redox transformations of P700 was monitored by changes in the magnitude of the low-field extremum of the first derivative of the EPR signal from \({\text{P}}_{{700}}^{ + }\). Illumination conditions and EPR signal recording in plant leaves were described in [54].

RESULTS AND DISCUSSION

Induction of Chlorophyll a Fluorescence

Fast induction of fluorescence. The kinetic curves shown in Fig. 1 were obtained on die-cuts from the leaves of plants acclimated to the conditions of strong or moderate illumination. Before starting the measurements, each sample was adapted to the darkness for 10 min. All FIF curves were normalized to the maximum value Fm of the signal. These curves had common patterns: in response to a short flash of intense light with λmax = 475 nm, the fluorescence of Chl a quickly reached the level F0 and then grew to the maximum level P, characterized by the parameter Fm, passing through inflection points or local extremes marked with the symbols J and I. After reaching the maximum P level, fluorescence slightly decreased. According to the generally accepted view, the O–J growth stage reflects the recovery of the primary plastoquinone PQA, which is tightly bound to PS2 [45–48]. The next phase of the signal growth (section J–I–P), called the “thermal phase” of fluorescence [56, 57], reflects the reduction of the secondary plastoquinone PQB (electron transfer PQA → PQB) and further electron transfer to the ETC between PS2 and PS1, as well as the redistribution of absorbed energy between PS2 and PS1 [58]. Comparing the kinetics of FIF in the leaves of the shade-tolerant species T. fluminensis in plants acclimated to strong or moderate light for 2 months, we can note that in the first case, the initial level of fluorescence F0 was higher than that of the leaves of the same species acclimated to a moderate light intensity. Considering that the parameter F0 reflects the efficiency of energy transfer from the light harvesting antenna to the reaction center P680 [48], it can be assumed that the observed difference was a consequence of damage to the PS2 antenna during exposure of T. fluminensis leaves to strong light (light stress). This did not happen in the case of the leaves of the light loving species T. sillamontana, which may indicate a relatively weak susceptibility of plants of this species to increased light intensity during acclimation. The parameters of the FIF curve depended on the duration of acclimation of plants under different illumination conditions (Fig. 3). We conducted the observations of the fluorescent indicators of leaves in vivo (without separation of leaves from the stem) during the long-term cultivation of plants (more than 4 months), starting from the two-week age of the leaves, when the plants have already formed leaf blades. Figure 3a shows the results of measurements in the experiment when, at first, plants grew under moderate illumination (50–125 µmol photons m–2 s–1) for 80 days, and then they were illuminated with strong light (850–1000 µmol photons m–2 s–1) of the same spectral composition. It can be seen that in both species the parameter F0 remained almost unchanged when plants grew under light of moderate intensity. After a significant (by an order of magnitude) increase in the light flux, the dependences of F0 on the acclimation time of the leaves of T. fluminensis and T. sillamontana changed. In the leaves of T. fluminensis, parameter F0 began to increase as the duration of acclimation increased. Unlike T. fluminensis, in the leaves of T. sillamontana no statistically significant F0 increase was observed (Fig. 3a).

Fig. 3.
figure 3

Dynamics of changes in parameter F0 of the fast fluorescence induction curve measured in the leaves of T. fluminensis and T. sillamontana grown under “strong” and “moderate” illumination. Vertical lines are the standard deviation from the average values obtained for n = 4–8 measurements.

Full size image

Figure 3b shows the results of another series of measurements, in which the sequence of illumination conditions was the opposite: the plants first grew under strong light, and then the light intensity was weakened. In shade-tolerant plants (T. fluminensis), during the first 50 days of growth under strong light, parameter F0 slightly changed. Then the F0 value began to increase noticeably. The increase of F0, observed when plants were illuminated with strong light, was reversible. After the weakening of the light on the 80th day, F0 started to decrease, returning to the initial level. In the case of the light loving species T. sillamontana grown under strong light, initially there was a slight decrease in F0. It can be suggested that this was because with an excess of light during acclimation to strong light, plants had enough light quanta for optimal functioning, so it was “beneficial” for them to reduce the number of pigment–protein complexes in order to avoid negative consequences from light stress. After the light faded, as the plants acclimated, the value of F0 increased, returning to the initial level. The described changes in the parameter F0 reflected the processes of structural and functional reorganization of the PSA occurring during the acclimation of plants. At the same time, in both series of experiments (Figs. 3a and 3b), in the leaves of the shade-tolerant plant T. fluminensis, the fluorescent parameter F0 was more sensitive to variations in light intensity during acclimation than in the leaves of the light loving species T. sillamontana.

The interspecies difference in the dynamics of changes in the F0 value during acclimation was also characteristic of the variable fluorescence of Chl a, defined as the ratio Fv/Fm = (Fm − F0)/Fm. Figure 4 shows that in the leaves of T. sillamontana this ratio remained at the same level (Fv/Fm ≈ 0.78) regardless of the growing conditions of plants (strong or moderate light). This indicated that the maximum quantum yield of Chl a fluorescence in T. sillamontana chloroplasts remained high at both moderate and high light intensity. Another pattern was observed in the case of T. fluminensis, namely, growth of these plants under strong light led to a certain drop in variable fluorescence Fv/Fm, which reflected a decrease in the photochemical activity of PS2. The decrease in the Fv/Fm ratio was reversible, that is, after the attenuation of the light intensity during acclimation of T. fluminensis, this ratio returns to the initial value of Fv/Fm ≈ 0.78, characteristic of plants grown at moderate light intensities (Fig. 4b). Reversibility of the Fv/Fm attenuation effect that occurred when T. fluminensis were grown under strong light illumination might indicate the functional “flexibility” of the PSA of these plants, that is, the photochemical activity of chloroplasts was restored relatively quickly (within a few days) after a decrease in illumination.

Fig. 4.
figure 4

Dynamics of changes in the variable fluorescence parameter Fv/Fm of the fast fluorescence induction curve measured in the leaves of T. fluminensis and T. sillamontana plants grown under “strong” and “moderate” illumination. Vertical lines are the standard deviation from the average values obtained for n = 4–8 measurements.

Full size image

Non-photochemical quenching of fluorescence. The reversibility of the FIF parameters in T. fluminensis leaves occurring during acclimation of plants to light of various intensity (Figs. 3 and 4) indicated the functional flexibility of the PSA of these plants, which allowed protecting the PSA from light stress. The protection of the PSA from damage under excessive illumination (strong light) was manifested in an increase in the non-photochemical quenching of the excitation of Chl a molecules in the light harvesting antenna of PS2. The coefficient of non-photochemical quenching (the NPQ value) can be determined from the parameters of the slow fluorescence induction curve (SIF) shown in Fig. 2.

Figure 5 shows how the NPQ value changed during the illumination of T. fluminensis leaves with continuous actinic light, in plants acclimated for different times at high (SL, Fig. 5a) or moderate (ML, Fig. 5b) light intensity. The intensity of actinic light used in the recording of SIF was quite high, 800 µmol photons m–2 s–1, which corresponded in order of magnitude to the intensity of strong light used in the acclimation of plants. In the kinetics of NPQ growth shown in Fig. 5, several components can be distinguished that reflect different mechanisms of regulation of the light stages of photosynthesis. The reversible component of NPQ, denoted as qE (the so-called energy component), was characterized by a relatively rapid growth (~0.5–2 min). This component was related to the creation of a trans-thylakoid pH difference (ΔpH) when, as a result of acidification of the intrathylakoid space (lumen), when the regulatory protein PsbS was activated, thereby enhancing NPQ [59]. It is believed that the PsbS protein acts as a sensor that provides sensitivity to a light-induced decrease in intra-thylakoid pH (pHin). Following the rapid growth of the NPQ (qE component), a relatively slow component of NPQ (denoted as the qZ component [50–52]) was often observed. This stage of the NPQ growth could be explained by two main reasons: (1) the reactions of the xanthophyll cycle (de-epoxidation of violaxanthin and the appearance of zeaxanthin) and (2) the redistribution of energy between PS2 and PS1 (state 1 ↔ state 2 transitions) [24, 29]. Zeaxanthin enhances the binding of the regulatory protein PsbS to the light harvesting antenna of PS2 (LHCII). This causes aggregation of light harvesting complexes of PS2 (LHCII), which leads to an increase in NPQ; the energy dissipation of excited pigments of the PS2 antenna enhances and the efficiency of photochemical processes in PS2 decreases (for more detail, see the review [29]). Based on our previous studies [34], it can be concluded that in the leaves of Tradescantia, the growth of NPQ was associated with an increase in the expression of the PsbS protein.

Fig. 5.
figure 5

The effect of the acclimation duration of T. fluminensis plants grown under strong (SL) and moderate (ML) light intensity on the kinetics of light-induced changes in the coefficient of non-photochemical fluorescence quenching (NPQ). Curves 1, 2, and 3 were obtained for plants acclimated to strong light for 8, 20 and 40 days. Curves 4 and 5 were obtained for leaves of plants acclimated to moderate light for 8 and 45 days. The intensity of continuous (actinic) light acting on the measured samples was 800 µmol photons m–2 s–1.

Full size image

After the actinic light was turned off, a decrease in NPQ was observed. The fall of the NPQ in the darkness was reversible, although not complete, namely, the residual level of NPQ remained comparatively long (tens of minutes), characterized by the parameter qI (Fig. 5). The value of qI is known to reflect, at least partially, the degree of inactivation of some of the photochemical centers of PS2 as a result of the action of sufficiently intense actinic light [30, 48–53]. The inhibition of PS2 occurred mainly due to damage to the D1 protein as a result of its photo-oxidation under the action of strong light. PS2 was repaired by the removing damaged protein D1 from PS2, and a newly synthesized active protein D1 was inserted in its place [60].

The ability of plants to enhance NPQ depended on the illumination conditions upon plant cultivation, as well as on the duration of acclimation. It is seen from Fig. 5a that with an increase in the duration of acclimation of T. fluminensis plants grown under strong light, a relatively small increase in the reversible (“energy”) component of qE was observed. It should be noted that as the plants aged, the contribution of the second (slow) component of NPQ (qZ) becomes more and more pronounced. This suggests that as the T. fluminensis leaves matured, their PSA acquired an additional ability to protect itself from light stress. Note that plants grown under moderate light also had two phases of NPQ growth (Fig. 5b), but the values of the qE and qZ parameters, reflecting the two mechanisms of NPQ generation, were slightly lower than those in plants grown under strong light (Fig. 5a). It is obvious that in plants grown under moderate light, the strengthening of the protective reaction caused by an increase in NPQ was less pronounced than in plants of the same species grown under strong light. Naturally, in strong light, plants have enough energy for photosynthesis, but at the same time they must protect themselves from light stress.

We have shown that the dynamics of NPQ changes during the illumination of Tradescantia leaves adapted to darkness depended on the duration of acclimation of plants to light of high or moderate intensity. This is especially evident in experiments with the shade-loving species T. fluminensis. In plants grown under strong light, the value of qE increased markedly with acclimation (Fig. 5a). At the same time, the slow qZ component became more pronounced. Obviously, the plants of the shade-loving type T. fluminensis, grown under strong light, acquired an additional ability to protect themselves from light stress during acclimation. As the acclimation time increased, this reaction of the PSA of plants became more pronounced. At the same time, when plants were exposed to light of moderate intensity for a long time, this did not happen, even a slight decrease in qE was observed as plants acclimated. It can be assumed that the decline in qE was caused by changes in chloroplasts as plants aged, which might be due, for example, to a decrease in biosynthesis and/or increased degradation of some PSA proteins.

Electronic Paramagnetic Resonance

Differences in the leaves of plants grown under strong and moderate illumination manifested in fluorescent characteristics were also expressed in the kinetics of redox transformations of P700, the primary electron donor in the reaction center of PS1. Figure 6 shows the typical curves of photoinduced changes in the intensity of the EPR signal from \({\text{P}}_{{700}}^{ + }\) in the leaves of plants adapted to darkness for 10 min. The protocol of \({\text{P}}_{{700}}^{ + }\) measurement was the same as in our previous studies [54, 55]: after preliminary illumination with white light (WL) for 1 min (to standardize experimental conditions), the samples were adapted to the darkness for 10 min. It can be seen that in response to the WL exciting both photosystems, the EPR signal from \({\text{P}}_{{700}}^{ + }\) increased, reaching a stationary level. In leaves adapted to the darkness, a multiphase kinetics of signal growth was observed. Immediately after switching on the WL, a small jump in the signal occurred, then its relatively slow growth to the stationary AWL level was observed. The delay in the signal growth, characterized by the t1/2 parameter, was because, when the leaf adapted to darkness, the CBC reactions were inactivated, therefore, due to an overabundance of NADPH, the outflow of electrons from PS1 to NADP+ was hindered [10, 61]. As the chloroplasts were illuminated, CBC reactions were activated and the outflow of electrons from PS1 accelerated. In addition, the rate of electron influx from PS2 to \({\text{P}}_{{700}}^{ + }\) decreased as a result of lumen acidification, and the activity of PS2 decreased due to the generation of NPQ. Along with this, the energy of the absorbed light was redistributed in favor of PS1 (transition state 1 → state 2), and there was a redistribution of electron flows (non-cyclic /cyclic electron transport) in favor of a non-cyclic flow [61]. All this should contribute to the growth of the EPR signal from \({\text{P}}_{{700}}^{ + }\).

Fig. 6.
figure 6

Kinetics of photoinduced changes in the amplitude of the EPR signal from \({\text{P}}_{{700}}^{ + }\) in the leaves of T. fluminensis and T. sillamontana grown under illumination with strong (SL) or moderate (ML) light. Before switching on the white light (WL), the samples were adapted to the darkness for 10 min.

Full size image

Figure 6 also shows that the rate of oxidation of P700 under WL depended on the conditions of plant growth. In both species of Tradescantia acclimated to strong light, photooxidation of P700 occurred noticeably faster than in plants grown under moderate light.

After switching from the WL to a weaker far-red light (FRL, λmax = 707 nm), which excited mainly PS1, the concentration of \({\text{P}}_{{700}}^{ + }\) dropped but then monotonically increased. The rapid drop in the signal after switching from the WL to FRL is explained by the influx of electrons to \({\text{P}}_{{700}}^{ + }\) from the pool of reduced carriers (these are mainly plastoquinol molecules) accumulated in the ETC between PS2 and PS1 during the action of the WL. The characteristic decay time of the signal from \({\text{P}}_{{700}}^{ + }\) after switching off the WL was t1/2 ~ 5–30 ms (depending on the duration of the WL action, data are not presented), which corresponded to the electron transfer time from plastoquinol to \({\text{P}}_{{700}}^{ + }\) [1, 4–6, 62–64]. After the reoxidation of the ETC carriers between PS2 and PS1 due to the work of PS1 excited by the FRL, the signal from \({\text{P}}_{{700}}^{ + }\) increased again. After switching off the FRL, the oxidized \({\text{P}}_{{700}}^{ + }\) centers were reduced by endogenous electron donors [48, 49]. Reduction of \({\text{P}}_{{700}}^{ + }\) after switching off the FRL occurred several orders of magnitude slower (t1/2 ~ 2–5 s) than after switching off the WL (see the results of our research described in [64] for more details).

In the pattern described above, the acceleration of photooxidation of P700 in the leaves of plants grown at high light intensity, usually manifested in the kinetics of the SIF in the leaves of T. fluminensis and T. sillamontana. Earlier, in the studies of the effect of growth conditions (light intensity) on the kinetics of the SIF, we found that in the leaves of these plants grown under strong light, the SIF declined faster than in the leaves of plants grown at moderate light intensity [65]. The acceleration of the fluorescence decay of Chl a during the induction period might be due to the same regulatory mechanisms as the acceleration of photooxidation of P700 under the WL, namely, due to light-induced activation of CBC reactions, increased NPQ, ionic regulation of electron transport between PS2 and PS1, transitions like state 1 ↔ state 2, etc. (for review, see [66–68]). It is obvious that the patterns characteristic for the kinetics of redox transformations of P700 and for the SIF in the leaves of plants acclimated to strong and moderate light reflected the fact that, as a result of acclimation of plants to strong light, their PSA reacted faster to illumination fluctuations, and therefore these plants could successfully withstand light stress.

It should be noted that the ratio of the amplitudes of the EPR signals from the oxidized \({\text{P}}_{{700}}^{ + }\) centers induced by WL and FRL (parameters AWL and A707) depended on the species of plants and their growth conditions. The AWL/A707 ratio was slightly higher for T. fluminensis leaves grown under high light compared to plants grown under low light (Fig. 6a). As we suggested earlier [65], this might indicate that in the leaves of T. fluminensis, acclimated to strong light, the contribution of cyclic electron transport around PS1 increased, which was manifested under FRL, which excited predominantly PS1. No such difference was observed in the case of T. sillamontana leaves. The exact reasons for this are still unknown.

Thus, the leaves of both studied species of Tradescantia, cultivated under different light intensities, showed differences in the kinetics of photoinduced changes in P700. The main difference concerns the oxidation rate of P700 upon the WL illumination. For example, as the leaves of the shade-tolerant species T. fluminenesis, grown under moderate light, aged, the oxidation of P700, induced by the WL, slowed down (Fig. 7). At the same time, the leaves of the same plant species grown under strong light showed a faster rate of photooxidation of P700 compared to plants acclimated to moderate light. This means that the PS1 of plants grown under strong light reacted faster to the turning on the WL, which was consistent with the data of fluorescent studies.

Fig. 7.
figure 7

Dependence of the kinetic parameter t1/2 characterizing the rate of photooxidation of P700 under the white light (see the determination of t1/2 in Fig. 6) in the leaves of T. fluminensis, depending on the duration of acclimation of plants to light of strong and moderate intensity. Closed and open symbols correspond to the data obtained for different series of experiments.

Full size image

The question on how the quantitative composition of electron transport complexes and pigments of light harvesting antennas of PS1 and PS2 changed during prolonged acclimation of tradescantia to light of different intensity requires special analysis. According to our preliminary data, in both types of Tradescantia acclimated to strong light, the total content of Chl a and Chl b, relative to the unit mass of the green leaf, decreased (the data will be presented in our next paper). This observation is in good agreement with the literature data that in the leaves of other plant species, the relative sizes of the light harvesting antenna of PS2 decreased when plants were acclimated to strong light [25–27, 33, 40, 66].

CONCLUSIONS

A comparative study of two contrasting species of Tradescantia showed a noticeable difference in the dynamics of changes in photosynthetic parameters of shade-tolerant (T. fluminenesis) and light loving (T. sillamontana) species during prolonged acclimation of these plants to light of strong and moderate intensity. A noticeable difference in the functioning of the PSA of these species was revealed, manifested during prolonged acclimation of plants (up to 5 months). In the light-tolerant species T. sillamontana, photosynthetic parameters of PSA changed relatively little when plants acclimated to light of varying intensity. Photosynthetic parameters of chloroplasts of the shade-tolerant species T. fluminenesis showed higher lability. The damage of their PSA with increasing light intensity was accompanied by an increase in NPQ, which was manifested as the duration of leaf exposure increased (Fig. 6). One of the most effective mechanisms for enhancing the protection of the PSA of Tradescantia leaves from light stress was an increase in the expression of the regulatory protein PsbS, leading to an additional increase in NPQ [33].