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Article

Effect of Some Herbicides on Primary Photosynthesis in Malva moschata as a Prospective Plant for Agricultural Grass Mixtures

by
Jaroslav Lang
1,
Miloš Barták
2,
Peter Váczi
2 and
Josef Hájek
2,*
1
Department of Agrotechnics, Research Institute for Fodder Crops, Zahradní 1, 664 41 Troubsko, Czech Republic
2
Laboratory of Photosynthetic Processes, Department of Experimental Biology, Faculty of Science, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(1), 10; https://doi.org/10.3390/agronomy14010010
Submission received: 10 November 2023 / Revised: 29 November 2023 / Accepted: 13 December 2023 / Published: 20 December 2023
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Abstract

:
Musk mallow (Malva moschata) is a perennial European plant that grows in pastures and grass mixtures. M. moschata is a medicinal plant with a high content of polysaccharides, flavonoids, and other biologically active compounds. The sensitivity of the species to herbicides is, however, generally unknown. In our study, we investigated the effects of three herbicides with different active compounds: (1) Propaquizafop (PPQ), (2) Clopyralid (CPR), (3) Metamitron+Quinmerac (MMQ) on primary photosynthetic processes of M. moschata plants cultivated in two different temperatures (12 and 18 °C). Non-photochemical quenching (NPQ) of absorbed light energy by chlorophyll molecules and the parameters derived from fast chlorophyll fluorescence transient (OJIP) were evaluated before and then 1, 2, 5, 24, and 48 h after the herbicides application. Among the herbicides, only MMQ negatively affected the functioning of photosystem II (PSII). The effect, however, was reversible, and the plants reached pre-application values after 48 h. No herbicide-induced changes in NPQ were found over the time after the application. The majority of the OJIP-derived chlorophyll fluorescence parameters were found to be temperature-sensitive. The herbicides tested in our study may be ranked among those with only limited effects on primary photosynthetic processes in PSII. While the application of PPQ and CPR did not bring any negative effects on the functioning of PSII, MMQ application induced a decrease in the potential quantum yield of PSII (FV/FM) and activation of protective mechanisms, increased heat dissipation in particular. These changes, however, were fully alleviated 48 h after MMQ application.

1. Introduction

Aromatic medicinal plants are rich in a wide variety of compounds with antioxidant potential and a high capability to scavenge free radicals formed during antistress plant response [1]. These compounds comprise several groups. Polyphenolic compounds, polysaccharides, flavonoids, and several other biologically active compounds are found in Malva sp. (see [2] for review). Recently, compounds with biological activities isolated from M. sylvestris were studied, and their potential for pharmaceutical products was evaluated [3]. It has been reported that M. sylvestris is rich in polyphenols [4] and flavonoids [5] that play an important role in ethnomedicine as well as in pharmaceutical products. However, a comprehensive study on these compounds in M. moschata is still missing. The only exception is the study of [6] focusing on the content of carotenoids and photosynthetic pigments in M. moschata. Polysaccharides are other bioactive compounds in M. moschata with bioadhesion properties that have been studied [7]. The bioadhesion is promising for future medicine and biotechnologies. A range of biological activities of polysaccharides extracted from Malvaceae might be even wider since the anti-inflamatory activity was reported for leaf- and fruit-extracted mucilage ([8] Malva parvifolra, [9] Malva sylvestris, [10] Malva aegyptica).
Herbicide effects on photosynthesis of crops and agriculture-important plants are widely studied. Among the methods applied in such studies, those based on chlorophyll fluorescence have become increasingly exploited because of nonintrusive measurements, and due to short-term techniques, a number of repetitive measurements are carried out both in the field and in laboratory-based experiments [11]. Therefore, a relatively large data set of parameters might be obtained in a short time and under constant environmental conditions. In the majority of studies exploiting chlorophyll fluorescence, herbicide effects are evaluated by the changes in potential (e.g., [12]) and effective quantum yields (e.g., [13]) of photosynthetic processes. Much less attention, however, is devoted to the herbicide effects on the activation of protective mechanisms in leaf photosynthetic apparatus, chloroplast in particular. These changes are typically accompanied by increased antioxidative defense exploiting increased synthesis of antioxidative substrates and enzymes [14], structural changes in pigment-protein complexes forming light-harvesting complexes, and PSII supercomplex. Activation of the protective mechanisms results in an increase in non-photochemical quenching, i.e., utilization of absorbed light energy in the processes that are not involved in the photosynthetic linear electron transport chain. Surprisingly, the effect of herbicides on non-photochemical quenching and related processes has been studied only scarcely in crops and agriculturally important plants (e.g., Lactuca sativa, [15,16]), while a great number of studies exist in model plants.
For evaluation of herbicide-induced stress in photosynthetic apparatus, photosystem II (PSII) in particular, chlorophyll fluorescence measurements are used quite frequently, especially in crops [17]. In our study, we used two major techniques: (1) Fast chlorophyll fluorescence transients (OJIP curves) and (2) evaluation of non-photochemical quenching (NPQ, a proxy of protective mechanism activated by a stressor). The OJIP is a polyphasic rise of chlorophyll fluorescence measured during a 1–2 sec exposition of predarkened plant materials to light. Individual phases relate to particular processes in photosystem II. The first one is a photochemical phase (O–J) that relates to the balance between the reduction in photosystem II (PSII) primary electron acceptor (QA) and its reoxidation by QB (e.g., [18]). The second one, the J–I–P phase, is the thermal phase. The shape of the J-I-P phase shape depends on the temperature of measurement (see, e.g., [19]). The last phase is the P-step (peak) which is reached typically at 1.0–1.5 sec of the exposition to light and may split into G and H peaks [20]. Both shapes of OJIP and OJIP-derived chlorophyll fluorescence parameters provide an important information about the stress-induced negative effects in PSII. For herbicides, a vast number of studies addressed the negative effects of DCMU (a blocker of photosynthetic linear electron transport chain) both in the laboratory and field studies. The studies focusing OJIP-based evaluation of negative effects of the herbicides used in agronomy on focusing plant photosynthetic characteristics are less frequent but their number increases [21].
The second chlorophyll fluorescence technique used in our study was the evaluation of non-photochemical quenching (NPQ) in plants exposed to light. In general, NPQ is used to assess the involvement of other than photosynthetic pathways of deexcitation of energized PSII. These pathways consisting of energy-dependent, transistory, and photoinhibitory components of NPQ are considered protective mechanisms. NPQ helps a plant dissipate surplus light energy absorbed in LHCs and RCs and thus prevents reactive oxygen species (ROS) formation in photosynthesizing plant tissues. NPQ is a frequently used method to evaluate the effects of herbicides on the functioning of PSII, particularly the activation of photoprotective mechanisms [22]. Therefore, NPQ has recently been used in plants, including crops and weeds, for the evaluation of their sensitivity/resistance to particular herbicides (e.g., [23] for soybean and cotton, [24] for two weed species) and a marker for optimized photosynthesis and biomass production [25].
Malva moschata is a promising species for permanent grass mixtures. From a forage point of view, attention is paid to its role in permanent grasslands. The addition of M. moschata is important in terms of biodiversity and the quality of forage in the stand. For these reasons, musk mallow is included in our institute’s current research activity. This research focuses on the development of effective seed-production technology, germination tests at different temperatures, assessing the effect of herbicide treatments, determining the optimum number of harvests, and the proportion of M. moschata in grass mixtures. Our article focuses on the effect of herbicides.
The aim of our study was to evaluate the effects of selected herbicides on the primary photosynthetic processes of Malva moschata grown at low (12 °C) and high temperatures (18 °C) in order to suggest their optimum application in the field at different parts of vegetation season. We hypothesized that, among the tested herbicides, MMQ would have the most pronounced negative effect on primary photosynthetic processes since metamitron, an effective compound, is an uncoupler limiting functioning of photosystem II (PSII).

2. Materials and Methods

2.1. Cultivation and Experimental Conditions

Musk mallow (Malva moschata L.) seeds were treated at 70 °C for three hours before sowing. Our team obtained the seeds from the previous plant generation. The seeds and plants are a certified variety. After the temperature treatment, germination and emergence are more uniform. After temperature treatment, the seeds were sown in RS I substrate (supplier Agro profi, Říkov, Czech Republic) with the following composition: 70% of white peat, 30% of black peat, 20 kg m−3 bentonite. Chemical characteristics were as follows: pH (H2O) 5.5–6.5, N 190 ± 20 mg L−1, P2O5 200 ± 18 mg L−1, K2O of 220 ± 23 mg L−1.
The sown seeds were cultivated in 6 × 5.7 × 5 cm planters in a greenhouse for 54 days with a temperature regime of 15/10 °C. The two temperatures regimen mimicked two scenarios of spring season climate. Then, the plants were transferred to air-conditioned chambers with the following cultivation conditions set as follows: light/dark—16/8 h, temperature—18/12 °C, relative humidity—70/50%, light flux—210 μmol m−2 s−1. After three days, the experimental conditions were set. Temperatures were set to be as close as possible to field conditions during herbicide application. Cool variant: light 16/8 h, temperature 16/11, relative humidity 70/50, light flux 210 μmol m−2 s−1. Warm variant: light 16/8 h, temperature 25/19 °C, relative humidity 70/50%, light flux 210 μmol m−2 s−1. Four days after the experimental conditions were set, the cold variant was measured; for capacity and adaptation reasons, the warm variant was measured seven days after the experimental conditions were set.

2.2. Herbicide Application

Three different herbicides were chosen for the experiment, two of which are approved for use in the cultivation of Musk mallow (Malva verticillata L.). For the particular herbicides, their active substances are:
(1)
Propaquizafop (Propachizafop), i.e., (2-(propan-2-ylidenamino)oxyethyl (2R)-2-[4-(6-chlorchinoxalin-2-yl)oxyphenoxy]propanoate (a dose of 100 g·L−1, resp. 4.5 mL·L−1), recommended application dose: 1.35 L·ha−1 per 300 l of water.
(2)
Clopyralid, i.e., 3,6-dichloropyridine-2-carboxylic acid (a dose of 0.999 mL·L−1), recommended application dose: 0.3 L·ha−1 per 300 L of water.
(3)
Metamitron—525 g (4-amino-4,5-dihydro-3-methyl-6-phenyl-1,2,4-triazin-5-one), Quinmerac—40 g (7-chloro-3-methylquinoline-8-carboxylic acid), (a dose of 3.3 mL·L−1) recommended application dose: 1.0 L·ha−1 per 300 L of water.
In the following text, the three herbicides and their active compounds are abbreviated as follows: (1) PPQ, (2) CPR, and (3) MMQ.
The herbicides have different modes of action. MMQ, specifically its effective chemical metamitron, is a photosynthetic linear electron transport chain inhibitor. It uncouples the chain between PSII and quinon B (QB). Clopyralid, an effective chemical of CPR, mimics the action of the enzymes of the auxin group, which leads to disruption of plant cells and heavily disorganized plant growth, ending with plant death. Cyclopyralid is highly soluble in water. PPQ mode of action is an inhibition of fatty acid synthesis in plant cells, thanks to the inhibition of acetyl-CoA carboxylase (ACCase). Blocking of fatty acid synthesis leads to a loss of cell membrane integrity, metabolite leakage, and ultimately cell death [26,27]. PPQ’s effective chemical is propaquizafop, a quinoxaline herbicide (containing the pyrazine fragment), which is a strong oxidizer that may interfere with photosynthetic processes [28]. A high PPQ-induced decrease in chlorophyll content is reported for Zea mays after foliar application of PPQ [29].

2.3. Measurements of Chlorophyll Fluorescence Parameters

Four plants from each experimental treatment, including the control, were measured using a FluorPen (PSI, Drásov, Czech Republic) fluorometer. The chlorophyll fluorescence measurements were always taken on the same leaf. OJIP and NPQ parameters were measured (for details, see below). Leaves were darkened for 5 min before each measurement to reach the state of fully open reaction centers of PSII. This was a sufficient time to stabilize photosystem II, as demonstrated using pre-experimental measurements. Measurements of each parameter were taken before treatment, then 1, 2, 5, and 24 h after treatment by the herbicides.

2.4. Non-Photochemical Quenching Induction

The NPQ values were measured using a standard protocol immediately before and repeatedly after the treatment by the herbicide’s application (1, 2, 5, 24, and 48 h). The measurements started with the measurement of background chlorophyll fluorescence (F0) at the end of a dark period. Then, a short saturating pulse of light (photosynthetically active radiation, PAR) was applied to measure maximum chlorophyll fluorescence (FM) in the dark-adapted state. Then, the leaves were exposed to PAR for 5 min to induce slow Kautsky kinetics of chlorophyll fluorescence (for the shape of the Kautsky and characterization, see Figure 1, e.g., [30]). During the light period, a sequence of 5 saturating pulses was applied to evaluate maximum chlorophyll fluorescence in a light-adapted state and, consequently, non-photochemical quenching (NPQ) using the below equation: NPQ = (FM − FM’)/FM’, where FM is maximum chlorophyll fluorescence achieved after a saturation pulse given at dark-adapted state, and FM’ is maximum achieved after a saturation pulse given at light-adapted state. In addition, effective quantum yield (ϕPSII) was calculated from FM’ values (LSS—see Figure 1) using the equation ϕPSII = (FM’ − FS)/FM’, where FS is a steady state chlorophyll fluorescence.

2.5. Fast Chlorophyll Fluorescence Transients

The effects of herbicides and cultivation temperature on primary photosynthetic processes were measured using OJIPs. The transients were induced using a 2 s-lasting pulse of red light [630 nm; 3000 μmol(photon) m–2 s–1] and recorded in the FluorPen memory. After a download to a PC, the following chlorophyll fluorescence parameters were calculated using a software: (1) Background chlorophyll fluorescence (F0, O point), (2) Chlorophyll fluorescence signal at J point, (3) FV/FM—maximum effective quantum yield of photochemical processes in PSII, (4) ABS/RC (absorption flux per reaction center—RC), (5) TR0/RC (trapping rate of energy per reaction center), (6) ET0/RC (electron transport flux per RC), (7) DI0/RC (thermal flux of dissipated excitation energy, and (8) PIABS (performance index, i.e., the potential for energy conservation from exciton to the reduction in the plastoquinone pool. The above-specified OJIP-derived parameters [31,32] (Table 1).

2.6. Statistical Analysis

Statistical analysis was performed using the Statistica software v. 14.0 (TIBCO Software Inc., Palo Alto, CA, USA). Significant differences between the experiments of the treatments (herbicides, time after the application) were evaluated using factorial ANOVA and Fisher’s least square differences test at alpha = 0.05.

3. Results

The plants treated with PPQ and MMQ showed no increase in NPQ (see NPQ_Lss in Figure 2), while the CPR treatment at 18 °C led to an increase in NPQ followed by a decrease found 24 h after herbicide application. This behavior, however, did not differ from the untreated control (at 18 °C). NPQ values (Figure 2) derived from particular saturation pulses (1–5, abbreviated as L1 to Lss) were found to be the lowest in the L1 group, i.e., 60 s after the actinic light was switched on. This means that the processes forming NPQ were not fully activated and increased with the duration of actinic light: gradually in low temperature- and rapidly in high temperature-treated plants (for more details, see Section 4 Discussion). The time-response curves for NPQ (steady state value, NPQ_Lss, black symbols in Figure 2), however, were found to be herbicide-specific and cultivation temperature-dependent. They showed three different shapes: (1) a plateau formed by more or less constant NPQ values found 1, 2, 5, 24, and 48 h after a herbicide application (e.g., MMQ in low-temperature cultivated plants), (2) a decrease in NPQ values with the time after the herbicide application, and (3) an increase in NPQ followed by a decrease after the peak found either early (2 h) or later (24 h) after the herbicide application (control plants grown at high temperature, and CPR-treated plants grown at high temperature, respectively).
Among the chlorophyll fluorescence signals derived from the OJIP curves, both F0 and FJ responded sensitively to MMQ application but not to the other herbicides tested (see Figure 3). A rapid increase in F0 and FJ was witnessed within the first hours (1, 2 h) after the application, while a consecutive decline in F0 and FJ values was apparent over the course of time after the application. After 48 h, F0 and FJ values were close to the initial values before application. The effect of cultivation temperature was seen for the FJ chlorophyll fluorescence signal (Figure 3, lower left subpanel). For control plants, significantly higher FJ was reached in high temperature-treated plants, as well as those treated using PPQ application. In contrast, the plants treated using CPR exhibited higher FJ values in low- than high-temperature cultivated plants.
For untreated control plants as well as herbicide-treated plants, FV/FM was found to be significantly higher in the plants cultivated at higher than low temperatures (Figure 4). The most pronounced difference was apparent for control and Lotrel-treated plants. The negative effects of herbicides were seen only in MMQ-treated plants since FV/FM declined rapidly within the first few hours after MMQ application. However, the decrease was followed by a recovery that reached 48 h after MMQ application. In PPQ-treated plants, a contradictory response of FV/FM was reached after the herbicide application in the plants cultivated at different temperature. It decreased with time after application in plants grown at high temperatures but increased in plants grown at low temperatures. Similar responses to the herbicide treatment as reached for FV/FM were also gained for photosynthetic electron transport per RC of PSII (ET0/RC, Figure 5), suggesting that both potential and actual photosynthetic processes in PSII of M. moschata were affected by the three herbicides in the same way. Absorption of light energy by PSII was found to be constant and growth temperature-independent on control plants.
The application of herbicides led to a rather ambiguous response. CPR caused no change in ABS/RC, while scattered ABS/RC data with no clear trend were obtained for MMQ application. Surprisingly, the stimulative effect of PPQ application was seen with time in the high-temperature cultivated plants, while the opposite was true for the plants cultivated in low temperatures.
The limitation of photosynthetic processes caused by MMQ application was accompanied by an increase in thermal dissipation from PSII (DI0/RC). Control plants and those treated using PPQ and CPR did not show any increase in DI0/RC that is associated with herbicide-induced stress to PSII. There was; however, an apparent effect of cultivation temperature on the DI0/RC values: Thermal dissipation of absorbed light energy was higher in low- than high-temperature grown plants. The trapping rate (TR0/RC) showed the effect of cultivation temperature as well. Except for the MMQ-treated plants where no difference was found, TR0/RC values were always higher in high- than low-temperature-treated plants. A statistically significant decrease in TR0/RC was found in the low-temperature cultivated plants treated using PPQ. Performance index showed that, among the tested herbicides, only MMQ application led to a negative effect on PIABS during the first 5 h after application. Then, in the course of time, full recovery of PIABS was apparent.
The effective quantum yield of PSII (ϕPSII), an indicator of photosynthetic processes in the chloroplast, linear electron transport chain in particular, ending with ATP and NADPH formation, remained more or less unchanged by the herbicide treatments. The only effect was apparent after 1 h of exposition to a herbicide. In MMQ-treated plants grown at 18 °C, a decrease to about 50% of the initial (control) value was recorded. The negative effect of MMQ on ϕPSII was, however, reversible. Recovery of ϕPSII values to close-to-control level was seen 24 h after MMQ application. A similar response, i.e., ϕPSII decreased after 1 h of PPQ application, and consequent recovery was apparent in the plants grown at 12 °C.

4. Discussion

After the application of herbicides, the values of NPQ measured at each time gradually increased in the order of NPQ_L1, NPQ_L2, NPQ_L3, NPQ_L4 to NPQ_Lss in low temperature- but not high temperature-treated plants. This was caused by the fact that high-temperature-treated plants generally had higher NPQ mechanisms activated during long-term cultivation than the low-temperature-cultivated ones (c.f. first data points (before treatment) in low-temperature-cultivated to high-temperature-cultivated plants). Another reason is that activation of NPQ (protective physiological mechanisms) by experimental light during the measurements was slower in low- than high-temperature-cultivated plants. The latter is a general phenomenon related to a gradual increase in photochemical/non-photochemical quenching during the duration of actinic light, which is typically demonstrated by an increase in FM’ − FS (Lss) relative to FM’ − FS (L1) as shown earlier for higher plants and lichens as well [33]. This explanation might be supported by a gradual (curvilinear) increase in NPQ with time of exposition to experimental light, which has been documented for a variety of crops and agriculturally important plants by a photosynthetic induction method (in Hordeum vulgare [34] and in Solanum lycopersicum [35]).
The MMQ-induced increase in F0 and FJ can be explained as the herbicide-induced negative effects on the functioning of LHCII, PSII, and the secondary acceptor quinone B (QB), as well. The F0 and FJ increase is a well-described consequence of the action of several herbicides ([36,37] for FJ). An increase in FJ (in absolute values as well as relatively to peak value FP) is a typical consequence of the inhibition of PSII photochemical processes induced by a variety of stressors [38]. These negative changes in PSII, however, were found reversible in the course of time after the MMQ application, which means that the QB binding site was not occupied by the other molecules permanently (as known for molecular docking of DCMU and other urea-based molecules, [39]). The MMQ-induced uncoupling of the photosynthetic chain at the QB binding site, however, did not lead to permanent uncoupling of the linear electron transport chain and full inhibition of PSII processes. In our experiment, the exposition of experimental plants to MMQ led to only partial, short-term, and reversible inhibition of energy flow through PSII, which was reflected in FV/FM decline and recovery similar to the evidence reported by [37]. A herbicide-induced decline of FV/FM is well described for several herbicides of different modes of action applied in lab-based and/or filed experiments (e.g., [40], including MMQ [41]).
Metamitron (an MMQ component) is considered an inhibitor of photosynthetic electron transport [42]. The site of inhibition and the underlying mechanism of the electron transport suppression are not yet known satisfactorily [43]. Our data, however, indicate that MMQ can not be considered a permanent uncoupler of photosynthetic electron flow at the QB site. However, it is believed that metamitron stimulates state transition from PSII to PSI when PSII functioning is partly inhibited due to uncoupling at the QB site. Such changes unavoidably lead to a decrease in (ϕPSII) as a consequence of inhibition of photosynthetic electron transport rate (see Figure 6).
Recovery of FV/FM in MMQ-treated plants was found faster in the plants grown in high than low temperature, which might be associated with generally lower efficiency of primary photosynthetic processes in PSII at low temperature (compared to low-temperature plants) and adjustment (acclimation) of PSII and photochemical processes related to photosynthetic electron flow to low temperature. Application of MMQ led to the reduction in FV/FM in PSII in terms of hours. However, it was balanced by the NPQ increase. This suggests that the capacity of the activated non-photochemical quenching mechanism was sufficiently high and effective because PSII recovered its functioning 48 h after MMQ application. However, it still remains an open question which component of NPQ played a dominant role in the antistress response. The rate of recovery of FV/FM in the MMQ-treated plants to control (initial) values was consistent with the evidence reported for the peach leaves after foliar application of metamitron [44], indicating the metamitron doses used in our experiment were within physiological limits allowing fast and sufficient antistress response. Higher doses of metamitron cause prolonged recovery (in terms of days), as shown by [37] for sugar beets.
Those OJIP-derived parameters related to primary photosynthetic processes, as well as the performance index (PIABS), showed higher values in the plants grown at high temperatures. This means that the temperature optimum for photosynthesis, growth, and biomass formation in M. verticillata is equal to or higher than 18 °C. Herbicide effect on OJIP-derived parameters was apparent only for MMQ, specifically in electron transport rate (ET0/RC), performance index (PIABS), and thermal dissipation (DI0/RC) recorded 1–5 h after MMQ application. Moreover, an increase in FJ (see Figure 3 for MMQ) is indicative of herbicides’ effects on over-reduction in the photosynthetic apparatus in PSII related to inhibition of the transfer of electrons from QA to QB (see, e.g., [45]. Since increased DI0/RC is associated with a variety of stressors, including herbicides [46], it might be stated that the MMQ application activated the protective mechanism of PSII, leading to the evolution of absorbed excess energy as heat emission.

5. Conclusions

It is well established that herbicides applied in agronomy have different modes of action. They could interact directly with (1) photosynthesis (i.e., inhibitors of photosystem I and II), (2) carotenoid synthesis (via herbicide-induced inhibition), and may cause (3) reactive oxygen species (ROS) generation with consequent lipid peroxidation (uncouplers and inhibitors of protoporphyrinogen oxidase). The herbicides tested in our study may be ranked as those having only limited effects on primary photosynthesis and PSII.
NPQ showed a temperature-dependent response but not herbicide-dependent response. At 18 °C, NPQ values were found to be even lower than in untreated control, which indicates no herbicides-induced activation of protective mechanism at the level of primary processes of photosynthesis. However, negative changes were apparent in MMQ-treated plants at the PSII level. These changes comprised an increase in background chlorophyll fluorescence (F0) and FJ. They were indicative of less effective functioning of PSII (decrease in FV/FM) and resulted in a decrease in photosynthetic electron transport and an increase in thermal dissipation of absorbed light energy from PSII. Therefore, it might be concluded that, among the tested herbicides, MMQ had a negative (but reversible in terms of tens of hours) effect on PSII, while the other two herbicides did not. In general, the three herbicides, specifically their concentrations used for foliar application in this study, can be recommended for application in Malva moschata stands.

Author Contributions

Conceptualization—J.L. and M.B.; methodology—J.L.; investigation—J.L.; data curation—P.V. and J.H.; writing—original draft preparation—M.B. and J.H.; writing—review and editing—M.B., P.V. and J.H.; funding acquisition—J.L. All authors have read and agreed to the published version of the manuscript.

Funding

The research reported in this study was supported by the project CZ.01.1.02/0.0/0.0/20_321/0025202 within the Operation Programme PIK, provided by Ministry of Industry and Trade, Czech Republic.

Data Availability Statement

The data presented in this study are available in article.

Acknowledgments

This study was supported by the project CZ.01.1.02/0.0/0.0/20_321/0025202.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Record of chlorophyll fluorescence (Kautsky kinetics with saturation pulses) used for non-photochemical quenching (NPQ) evaluation presented for untreated control M. moschata plants ((A)—left) and those exposed to MMQ (Metamitron+Quinmerac) for 1 h ((B)—right). The arrows indicate maximum chlorophyll fluorescence levels (FM’—see Material and methods) reached after consecutive saturation pulses. The particular FM’ values were achieved after the application of particular saturation light pulses (L1 to Lss) and used for NPQ_L1, NPQ_L2, NPQ_L3, NPQ_L4, and NPQ_Lss calculation (see Figure 2). Note the MMQ-induced increase in overall chlorophyll fluorescence values throughout the Kautsky kinetics and the decrease in FM’ (relative to a steady-state chlorophyll fluorescence: FS) in MMQ-treated plants (B). These changes are indicative of negative effects in PSII.
Figure 1. Record of chlorophyll fluorescence (Kautsky kinetics with saturation pulses) used for non-photochemical quenching (NPQ) evaluation presented for untreated control M. moschata plants ((A)—left) and those exposed to MMQ (Metamitron+Quinmerac) for 1 h ((B)—right). The arrows indicate maximum chlorophyll fluorescence levels (FM’—see Material and methods) reached after consecutive saturation pulses. The particular FM’ values were achieved after the application of particular saturation light pulses (L1 to Lss) and used for NPQ_L1, NPQ_L2, NPQ_L3, NPQ_L4, and NPQ_Lss calculation (see Figure 2). Note the MMQ-induced increase in overall chlorophyll fluorescence values throughout the Kautsky kinetics and the decrease in FM’ (relative to a steady-state chlorophyll fluorescence: FS) in MMQ-treated plants (B). These changes are indicative of negative effects in PSII.
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Figure 2. Effects of herbicide application (0–48 h) on non-photochemical quenching (NPQ) in plants grown in low (upper panel) and high (lower panel) temperatures. Data points are means of 5 replicates with standard deviation indicated. Abbreviations of herbicides: PPQ (Propaquizafop), MMQ (Metamitron + Quinmerac), CPR (Clopyralid). Statistically significant differences (alpha = 0.05) were found for the following parameters (*): 12 °C, PPQ: NPQ_Lss: before (b), 1 h (b), 2 h (ab), 5 h (ab); 18 °C, control: NPQ_L1: 2 h (b), 5 h (ab); NPQ_L2: 2 h (b), 5 h (ab); NPQ_L3: 2 h (b), 5 h (ab); NPQ_L4: before (ab), 1 h (ab), 2 h (b), 5 h (ab); NPQ_Lss: before (ab), 1 h (ab), 2 h (b), 5 h (ab), 24 h (ab), 48 h (ab).
Figure 2. Effects of herbicide application (0–48 h) on non-photochemical quenching (NPQ) in plants grown in low (upper panel) and high (lower panel) temperatures. Data points are means of 5 replicates with standard deviation indicated. Abbreviations of herbicides: PPQ (Propaquizafop), MMQ (Metamitron + Quinmerac), CPR (Clopyralid). Statistically significant differences (alpha = 0.05) were found for the following parameters (*): 12 °C, PPQ: NPQ_Lss: before (b), 1 h (b), 2 h (ab), 5 h (ab); 18 °C, control: NPQ_L1: 2 h (b), 5 h (ab); NPQ_L2: 2 h (b), 5 h (ab); NPQ_L3: 2 h (b), 5 h (ab); NPQ_L4: before (ab), 1 h (ab), 2 h (b), 5 h (ab); NPQ_Lss: before (ab), 1 h (ab), 2 h (b), 5 h (ab), 24 h (ab), 48 h (ab).
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Figure 3. Effects of herbicide application (0–48 h) on selected chlorophyll fluorescence signals (F0—background chlorophyll fluorescence recorded at 0.01 μs, FJ—chlorophyll fluorescence signal recorded at 300 μs) derived from fast chlorophyll fluorescence transient (OJIP) in plants grown in low (blue symbols and lines) and high (red symbols and lines) temperature. Data points are means of 5 replicates with standard deviation indicated. Abbreviations of herbicides: PPQ (Propaquizafop), MMQ (Metamitron+Quinmerac), CPR (Clopyralid). Statistically significant differences (alpha = 0.05) are indicated by the letter b (the latter a is not shown).
Figure 3. Effects of herbicide application (0–48 h) on selected chlorophyll fluorescence signals (F0—background chlorophyll fluorescence recorded at 0.01 μs, FJ—chlorophyll fluorescence signal recorded at 300 μs) derived from fast chlorophyll fluorescence transient (OJIP) in plants grown in low (blue symbols and lines) and high (red symbols and lines) temperature. Data points are means of 5 replicates with standard deviation indicated. Abbreviations of herbicides: PPQ (Propaquizafop), MMQ (Metamitron+Quinmerac), CPR (Clopyralid). Statistically significant differences (alpha = 0.05) are indicated by the letter b (the latter a is not shown).
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Figure 4. Effects of herbicide application (0–48 h) on the OJIP-derived chlorophyll fluorescence parameters: Potential quantum yield of photochemical processes in PSII (FV/FM), absorption of light energy per reaction center (ABS/RC), thermal dissipation of absorbed light energy from PSII (DI0/RC). Data points are means of 5 replicates with standard deviation indicated. Abbreviations of herbicides: PPQ (Propaquizafop), MMQ (Metamitron + Quinmerac), CPR (Clopyralid). Statistically significant differences (alpha = 0.05) are indicated by the letter b (the latter a is not shown).
Figure 4. Effects of herbicide application (0–48 h) on the OJIP-derived chlorophyll fluorescence parameters: Potential quantum yield of photochemical processes in PSII (FV/FM), absorption of light energy per reaction center (ABS/RC), thermal dissipation of absorbed light energy from PSII (DI0/RC). Data points are means of 5 replicates with standard deviation indicated. Abbreviations of herbicides: PPQ (Propaquizafop), MMQ (Metamitron + Quinmerac), CPR (Clopyralid). Statistically significant differences (alpha = 0.05) are indicated by the letter b (the latter a is not shown).
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Figure 5. Effects of herbicide application (0–48 h) on the OJIP-derived chlorophyll fluorescence parameters: Photosynthetic electron transport rate per reaction center (ET0/RC), Trapping rate per reaction center (TR0/RC), and Performance Index (PIABS). Data points are means of 5 replicates with standard deviation indicated. Abbreviations of herbicides: PPQ (Propaquizafop), MMQ (Metamitron + Quinmerac), CPR (Clopyralid). Statistically significant differences (alpha = 0.05) are indicated by the letter b (the latter a is not shown).
Figure 5. Effects of herbicide application (0–48 h) on the OJIP-derived chlorophyll fluorescence parameters: Photosynthetic electron transport rate per reaction center (ET0/RC), Trapping rate per reaction center (TR0/RC), and Performance Index (PIABS). Data points are means of 5 replicates with standard deviation indicated. Abbreviations of herbicides: PPQ (Propaquizafop), MMQ (Metamitron + Quinmerac), CPR (Clopyralid). Statistically significant differences (alpha = 0.05) are indicated by the letter b (the latter a is not shown).
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Figure 6. Effective quantum yield of photosynthetic processes in PSII (ϕPSII) for untreated control and the herbicides-affected plants of M. moschata. The plants were cultivated and exposed to PPQ (Propaquizafop), CPR (Clopyralid), and MMQ (Metamitron + Quinmerac) at low (12 °C) and high temperatures (18 °C). Statistically significant differences (alpha = 0.05) are indicated by the letters abc, ab, b, bc, c (the latter a is not shown in the three subpanels in the upper row, and the three subpanels of the lower row. In these subpanels, there is no statistical difference in ΦPSII values evaluated for control, and the particular time after a herbicide application).
Figure 6. Effective quantum yield of photosynthetic processes in PSII (ϕPSII) for untreated control and the herbicides-affected plants of M. moschata. The plants were cultivated and exposed to PPQ (Propaquizafop), CPR (Clopyralid), and MMQ (Metamitron + Quinmerac) at low (12 °C) and high temperatures (18 °C). Statistically significant differences (alpha = 0.05) are indicated by the letters abc, ab, b, bc, c (the latter a is not shown in the three subpanels in the upper row, and the three subpanels of the lower row. In these subpanels, there is no statistical difference in ΦPSII values evaluated for control, and the particular time after a herbicide application).
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Table 1. List of the OJIP-derived parameters used in our study of selected herbicides (PPQ, CPR, and MMQ) and their effect on primary photosynthetic processes.
Table 1. List of the OJIP-derived parameters used in our study of selected herbicides (PPQ, CPR, and MMQ) and their effect on primary photosynthetic processes.
Abbrev.Formula/EquationsExplanation
F0 Background chlorophyll fluorescence (F0, O point)
FJ Chlorophyll fluorescence signal at J point
FV/FMFV/FM = (FM − F0)/FMMaximal quantum yield of PSII fluorescence
NPQNPQ = (FM − FM’)/FM’Non-photochemical quenching
PIABSPIABS = (RC/ABS) · [φP0/(1 − φP0)] · [ψ0/(1 − ψ0)]Performance index (potential) for energy conservation from exciton to the reduction in intersystem electron acceptors
ABS/RCABS/RC = M0(1/VJ)(1/φP0)Absorption flux (of antenna chlorophylls) per RC
TR0/RCTR0/RC = M0(1/VJ)Trapped energy flux (leading to QA reduction) per RC
ET0/RCET0/RC = M0 · (1/VJ) · ψ0Electron transport flux (further than QA) per RC
DI0/RCDI0/RC = (ABS/RC) − (TR0/RC)The flux of dissipated excitation energy at time 0
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Lang, J.; Barták, M.; Váczi, P.; Hájek, J. Effect of Some Herbicides on Primary Photosynthesis in Malva moschata as a Prospective Plant for Agricultural Grass Mixtures. Agronomy 2024, 14, 10. https://doi.org/10.3390/agronomy14010010

AMA Style

Lang J, Barták M, Váczi P, Hájek J. Effect of Some Herbicides on Primary Photosynthesis in Malva moschata as a Prospective Plant for Agricultural Grass Mixtures. Agronomy. 2024; 14(1):10. https://doi.org/10.3390/agronomy14010010

Chicago/Turabian Style

Lang, Jaroslav, Miloš Barták, Peter Váczi, and Josef Hájek. 2024. "Effect of Some Herbicides on Primary Photosynthesis in Malva moschata as a Prospective Plant for Agricultural Grass Mixtures" Agronomy 14, no. 1: 10. https://doi.org/10.3390/agronomy14010010

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