How photosynthetic light phase of spiny cocklebur (Xanthium spinosum L.) changes during times after herbicide application

Document Type : Research Paper

Authors

1 Department of Plant Eco-Physiology, University of Tabriz, Tabriz, Iran.

2 Dryland Agricultural Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Maragheh, Iran.

3 Dryland Agricultural Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Maragheh, Iran

Abstract

The photosynthetic light phase of spiny cocklebur (Xanthium spinosum L.) plant was studied by JIP-test at different times (12, 36, 60 and 84 hours) after nicosulfuron and bentazon herbicides application. Results indicated that application of nicosulfuron had no effect on the most of chlorophyll a fluorescence parameters. But, application of bentazon significantly decreased photosystem II (PSII) activity via increasing minimum fluorescence and decreasing maximum fluorescence, variable fluorescence, the activity of the water-splitting complex on the donor side of PSII and especially maximum quantum yield of PSII photochemistry. Application of bentazon had a greater effect on the donor site than on the acceptor site of PSII by increasing absorption flux per reaction center and decreasing the values of efficiency through which the trapped electrons from RCs continue beyond QA and also by reduction of quantum yield for electron transport from QA- to PQ. Reduction in photosynthesis relative vitality (PI) by application of bentazon negatively affected reaction centers per PSII antenna chlorophyll, maximum quantum yield for primary photochemistry and the quantum yield for electron transport. In most case, the inhibitory effects of bentazon on PSII activity were recorded at 36 hours after herbicide application. Bentazon treatment decreased the rate of the electron transport chain and this was supported by increasing the photochemical de-excitation rate constant in the excited antennae of energy fluxes for photochemistry.

Keywords


Introduction

 

Among all herbicides which are used in crop protection, nearly 50% affect the chloroplast. Several herbicides such as benzothiadiazinones are known as inhibitors of photosystem II (PSII) activity (Cobb and Read 2010). Bentazon (Basagran, SL48%) which belongs to the benzothiadiazinones is a very strong inhibitor (Grumbach 1982). This herbicide is used for the control of broadleaf weeds in crops such as corn and soybean (Cobb and Read 2010). Apart from inhibiting electron transport, many herbicides have more than one side of action. Photosystem II inhibitor herbicides like bentazon also alter chloroplast ultrastructure and pigment composition (Grumbach 1982). Nicosulfuron (Cruz, SC4%) is a sulfonylurea herbicide being considered for registration for post-emergence weed control in crops such as corn (Williams and Gilham 1990). Sulfonylureas are a class of herbicides that inhibit the activity of acetohydroxyacid synthase/acetolactate synthase and decrease the synthesis of valine, leucine and isoleucine as the branched- chain amino acid (Ray 1984; Cobb and Read 2010).

Many stresses such as herbicide application on plants can affect the photosynthetic activity of leaves and change the ChlF parameters )Oukarroum et al. 2007; Kalaji and Guo 2008; Hassannejad et al. 2020). ChlF analysis as a rapid, non-intrusive  and  inexpensive  method,  provides

 

 

detailed information on the energy flow in the photosynthetic apparatus (Oukarroum et al. 2007). This method can be used for understanding the stressful effects of herbicides on weeds (Hassannejad et al. 2020). Thus, the purpose of this experiment was to evaluate the photosynthetic light phase by JIP-test of chlorophyll a fluorescence in spiny cocklebur (Xanthium spinosum L.) plants as a noxious weed species present in corn (Zea mays L.), soybean (Glycine max L.), and some other summer crops after post-emergence application of nicosulfuron and bentazon herbicides.

 

Materials and Methods

Plant Materials and Growth Conditions

A pot experiment using a randomized complete block design with three replications was conducted in the glass greenhouse conditions under natural light (27-32 °C) in the University of Tabriz in 2017 to assess the effect of nicosulfuron and bentazon herbicides on spiny cocklebur (X. spinosum L.) chlorophyll a florescence (ChlF) parameters and PSII activity. Fifteen seeds of spiny cocklebur were sown in each plastic pot (20 × 20 cm) containing 1.0 kg of perlite at a depth of 1 cm and then tap water (0.6 dS m-1) was added to achieve 100% field capacity. Plants were thinned to 5 plants per pot, after seedling establishment. The losses of pots were made up with Hoagland solution (Electrical conductivity =1.3 dS m-1 and pH= 6.5-7) and every 20 days, water was added to prevent further increase in the electrical conductivity. Herbicides were applied at the 4-5 leaf stage of spiny cocklebur at the recommended dose in the field as 2 L.ha-1.

      ChlF parameters from the upper surface of spiny cocklebur leaves were monitored with a handy-PEA portable fluorometer (Hansatech, UK) after 12, 36, 60 and 84 hours of herbicide application. This device has software for calculation, numerical presentation and memorization of chlorophyll a fluorescence parameters (Table 1).

      All the data were analyzed based on the experimental design, using SAS 9.1 software. The means of each trait were compared using Duncan’s multiple range test at p≤ 0.05.

 

Results

Application of nicosulfuron and bentazon increased initial fluorescence (F0) of plants. Bentazon had a higher effect on F0 at all times after application as compared with nicosulfuron. However, in most cases, especially at 12 and 84 hours after application of nicosulfuron, the effect of this herbicide on F0 was similar to the control treatment. Maximum F0 was observed at 36 hours after bentaznon application (Figure 1a). Maximum fluorescence (Fm) was only affected by bentazon and the effect of nicosulfuron on Fm was not significant. Fm significantly declined with increasing the time after bentazon application, so that the lowest amount of this variable was observed at 84 hours (Figure 1b).

 

 

 

 

 

 

 

Table 1. ChlF parameters measured on spiny cocklebur after herbicides application.

Abbreviations

Description

ChlF

Chlorophyll a fluorescence

PSI

Photosystem I

PSII

Photosystem II

PI

Performance index

ETC

Electron transfer chain

QA

Primary electron acceptor in PSII

F0

Initial fluorescence

Fm

Highest fluorescence

Fv

Variable fluorescence

Fv/Fm

The maximum quantum yield of PSII photochemistry

Fv/F0

The activity of the water-splitting complex

Sm

The energy needed for the closure of reaction centers

Area

The area above the fluorescence induction curve between the minimum and maximum fluorescence for representing the size of the plastoquinone pool in photosystem II

Tfm

The time that takes to reach form F0 to Fm, for representing the QuinoneA reduction rate of the PSII acceptor

Sm/Tfm

The average redox state of QuinoneA in the period from F0 to Fm and concomitantly

VJ

Fv after 2 ms

VI

Fv after 30 ms

ABS/RC

Absorption energy flux in each reaction center

TR0/RC

Trapped energy in each reaction center

ET0/RC

Maximum electron transportation in each reaction center

DI0/RC

Dissipation energy flux in each reaction center

φ E0

Quantum yield for electron transportation from QuinoneA- to plastoquinone

ѱE0

The probability that trapped excitation moves an electron into the electron transport chain beyond QuinoneA-

φR0

Quantum yield of reduction of end electron acceptors at the PSII acceptor side

KN

The non-photochemical de-excitation rate constant in the excited antennae for non-photochemistry

KP

The photochemical de-excitation rate constant in the excited antennae of energy fluxes for photochemistry

 

 

 

Figure 1. Changes in F0 (a) and F0 (b) of spiny cocklebur (Xanthium spinosum L.) after 12, 36, 60 and 84 hours of nicosulfuron and bentazon herbicides application.

 

 

 

 

 

 

 

Fv/Fm was not affected by nicosulfuron, while significantly decreased by bentazon. As the time after bentazon application increased, the amount of Fv/Fm declined, so that the lowest Fv/Fm was obtained at 84 hours after bentazon treatment (Figure 2a). Bentazon harmed Fv/F0, but nicosulfuron only slightly influenced this variable. Treated plants by nicosulfuron had lower Fv/F0 than that of control plants and this reduction started at 36 hours after the treatment. However, Fv/F0 decreased significantly with increasing the time after bentazon application. Thus, the minimum amount of Fv/F0 was observed at 84 h after bentazon application (Figure 2b).

Variable fluorescence (Fv) was reduced after  

 

 

 

Figure 2. Changes in Fv/Fm (a) and Fv/F0 (b) of spiny cocklebur (Xanthium spinosum L.) after 12, 36, 60 and 84 hours of nicosulfuron and bentazon herbicides application.

 

 

bentazon application, and this reduction continued with increasing the time after the herbicide application (Figure 3a). Area slightly increased by the application of nicosulfuron, however, this increase was not significant at 12 and 60 hours after herbicide application. But, at 36 hours after bentazon application, Area decreased substantially (Figure 3b).

Sm and Sm/Tfm were significantly increased with the nicosufuron application. But, bentazon reduced Sm and it was not recovered after bentazon application (Figure 4a, b). Sm declined after 36 hours of the bentazon treatment and then remained unchanged (Figure 4a). However, the effect of bentazon on Sm/Tfm was not significant (Figure 4b).

The time taken to reach Fm (Tfm) was only affected by bentazon. Tfm in the bentazon treated plants at 12 hours after application was higher than that of other treatments; this variable was strongly reduced at 36 hours after herbicide application and then remained constant (Figure 5a). Photosynthesis relative vitality (PI) as an important chlorophyll a fluorescence parameter was strongly decreased by betnazon. PI in treated plants at 12 hours after bentazon application was close to zero and at 36 hours after this herbicide application had no activity. The negative effect of

 

 

 

 

 

Figure 3. Changes in Fv (a) and Area (b) of spiny cocklebur (Xanthium spinosum L.) after 12, 36, 60 and 84 hours of nicosulfuron and bentazon herbicides application.

 

 

Figure 4. Changes in Sm (a) and Sm/Tfm (b) of spiny cocklebur (Xanthium spinosum L.) after 12, 36, 60 and 84 hours of nicosulfuron and bentazon herbicides application.

 

 

 

nicosulfuron on PI was observed at 36 hours after

the herbicide application and after that time, this variable was not recovered significantly (Figure 5b).

Application of nicosulfuron after 12 h, caused a slight increase in KP but, after 36 h, it decreased KP in plants. However, application of bentazon after 12 h strongly decreased KP, and this reduction was more evident with increasing the time after bentazon application (Figure 6a). Application of nicosulfuron did not affect KN, however, bentazon strongly increased KN after 12 h of application and this enhancement was greater at 84 h after the bentazon treatment (Figure 6b).

The effect of both nicosulfuron and bentazon herbicides on other ChlF parameters was presented as a spider plot graph in Figure 7. Bentazon increased Fv at 2 ms (Vj) and especially increased the absorption of ABS/RC, and with increasing the time after bentazon application, these effects were more pronounced. In contrast, this herbicide decreased ET0/RC, ѱE0, φE0 and φR0.

 


 

Figure 5. Changes in Tfm (a) and PI (b) of spiny cocklebur (Xanthium spinosum L.) after 12, 36, 60 and 84 hours of nicosulfuron and bentazon herbicides application.

 

 

 

 

 

Figure 6. Changes in KP (a) and KN (b) of spiny cocklebur (Xanthium spinosum L.) after 12, 36, 60 and 84 hours of nicosulfuron and bentazon herbicides application.

 

 

However,   the   application   of  nicosulfuron did not affect the JIP parameters.

The lethal effects of an herbicide in higher plants depend on the particular side at which a physiological reaction is inhibited in a plant cell and its compartments. In the chloroplast, there are two main target sides of the herbicide action. One target is represented by the electron transport chain with its electron carriers and enzymes which are involved in phosphorylation and NADP photo-reduction. Another main target of the herbicide action is the biosynthesis of chlorophylls and carotenoids that are contained in the light-harvesting complex and the antennae of the photosynthetic reaction centers (Hassannejad et al. 2020; Baghbani et al. 2019). In our research application of bentazon in comparison with nicosulfuron strongly influenced PSII activity of spiny cocklebur plants. Bentazon enhanced F0 but decreased  Fm  of   plants   Figure 1). F0    is    the

 

 

 

Figure 7.Spider plot presenting the JIP-test parameters calculated from nicosulfuron (a) and bentazon (b) treated spiny cocklebur (Xanthium spinosum L.) plants.

 

 

 

fluorescence    level    when    plastoquinone  (PQ)

electron acceptor pool is fully oxidized and it may change upon exposure to stresses (Fracheboud et al. 2004). An increase in F0 can be interpreted as a reduction of the rate constant of energy trapping by PSII centers, which could be the result of a physical dissociation of light-harvesting complex from PSII core observed in several plant species under environmental stresses (Rong-hua et al. 2006). Reduction in Fm under bentazon application (Figure 1b) may have caused by the inhibition of electron transport at the donor side of the PSII (Hassannejad et al. 2020), which resulted in the Tfm decrease (Figure 5a).

Application of bentazon destructed the reaction centers of PSII in the treated plants (photo-chemically active), thus electron transport capacity in PSII and the number of quanta absorbed per unit time decreased. Bentazon treatment not only decreased protein kinase activity but also destructed D1 protein level and correspondingly, Fv/Fm, electron transfer rate (ETR) and photosynthetic rate were reduced (Figure 2a). Fv/F0 is the most sensitive component in the photosynthetic electron transport chain (Hassannejad et al. 2020). The decrease in Fv/F0 (Figure 2b) as a consequence of bentazon application, results from photosynthetic electron transport destruction, which affects the Sm/Tfm parameter in plants (Figure 4b). Bentazon inhibits the electron transfer rate at the donor side of PSII and the electron transportation from reaction centers to the plastoquinone pool and decreased Area (Figure 3b). Decreasing in Sm (Figure 4a) was the consequence of a decrease in Area (Figure 3b) and Fv (Figure 3a) under application of bentazon. Application of bentazon impaired both light and dark reactions of photosynthesis as a result of the reduction in PI (Figure 5b). Decreasing  in PI  may  be  related  to

 

 

the effects of bentazon on the density of reaction centers per PSII antenna chlorophyll, maximum quantum yield for primary photochemistry and the quantum yield for electron transport (Hassannejad et al. 2020).

      Bentazon strongly increased Vj and ABS/RC but decreased ET0/RC, ѱE0, φE0 and φR0 (Figure 7). As the ѱE0 values of bentazon samples were low, the electron carriers could not transfer electrons to the next step of the electron transport chain (Joshi et al. 1995; Toth et al. 2007; Lotfi et al. 2018;Hassannejad et al. 2020). After bentazon application, the PSII acceptor side was limited more than the PSII donor side as Lotfi et al. (2018) showed after humic acid application in rapeseed plants.

 

Conclusion

Bentazon belongs to the benzothiadiazinones and are known as PSII inhibitors and Nicosulfuron belong to the sulfonylurea a class of herbicides that by inhibiting the activity of acetohydroxyacid synthase/acetolactate synthase decreases the synthesis of branched-chain amino acids. According to the mode of action of the used herbicides, nicosulfuron did not affect the photosynthetic activity of the spiny cocklebur samples. However, bentazon strongly destroyed the photosystem II activity of spiny cocklebur. The donor side of PSII was more sensitive than its acceptor side to bentazon. This claim was supported by an increase in ABS/RC and a decrease in ѱE0 and φE0. After 12 h of bentazon application, the PI was close to zero and after 36 h the photosynthetic activity was completely destroyed.

 

Conflict of Interest

The authors declare that they have no conflict of interest with any organization in relation to the subject of the manuscript.

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