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Article

Control of Resistant False Cleavers (Galium spurium L.) Population to ALS-Inhibiting Herbicides and Its Impact on the Growth and Yield of Durum Wheat

by
Panagiotis Sparangis
1,
Aspasia Efthimiadou
2,*,
Nikolaos Katsenios
2 and
Anestis Karkanis
1,*
1
Department of Agriculture, Plant Production and Rural Environment, University of Thessaly, Fytokou St., 38446 Volos, Greece
2
Department of Soil Science of Athens, Institute of Soil and Water Resources, Hellenic Agricultural Organization-Dimitra, Sofokli Venizelou 1, Lycovrissi, 14123 Athens, Greece
*
Authors to whom correspondence should be addressed.
Agronomy 2023, 13(4), 1087; https://doi.org/10.3390/agronomy13041087
Submission received: 5 March 2023 / Revised: 4 April 2023 / Accepted: 9 April 2023 / Published: 10 April 2023
(This article belongs to the Section Weed Science and Weed Management)
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Abstract

:
False cleavers (Galium spurium L.) is an annual broadleaf weed, commonly found in cereal crops around the world. It reduces crop yields mainly by the competition for nutrients and plant lodging, which decreases the photosynthetic rate of cultivated plants. Two field experiments were carried out in different locations to examine the efficacy of post-emergence herbicides against false cleavers in durum wheat (Triticum durum Desf.). Herbicides that belong to sulfonylureas, triazolopyrimidines, and other groups (e.g., nitriles and synthetic auxins) were applied. The results revealed that the herbicide florasulam + aminopyralid provided low efficacy (57%) against this weed species, while the most effective herbicides were bromoxynil + 2,4-D and halauxifen-methyl + florasulam. Bromoxynil + 2,4-D efficacy against false cleavers was 73% and 97% at Domokos and Velestino, respectively, while halauxifen-methyl + florasulam efficacy ranged between 89% and 97%. Moreover, the herbicides metsulfuron-methyl + bensulfuron-methyl and pyroxsulam/florasulam + 2,4-D provided low efficacy (<11%) against false cleavers, revealing resistance to ALS-inhibiting herbicides. Regarding the impact of false cleavers and other weed species on the growth of durum wheat, the results showed that the greatest dry biomass (8508.3–8922.7 kg ha−1 and 13,041.4–13,523 kg ha−1 at Domokos and Velestino, respectively) was found in the bromoxynil + 2,4-D, halauxifen-methyl + florasulam, and weed-free treatments. Similar results were also recorded for 1000-seed weights and crop yields, while there were no statistically significant differences among the treatments for spike length. Finally, our results revealed that the herbicides bromoxynil + 2,4-D and halauxifen-methyl + florasulam effectively controlled the resistant false cleavers population. However, it is important to note that halauxifen-methyl + florasulam was recently registered in Greece and other countries and, thus, should be used sensibly by farmers in a rotation with other herbicides to prevent the development of resistant populations.

1. Introduction

Wheat cultivation has a leading role in the context of tackling the problem of global hunger, which is becoming more and more troubling as the population increases [1]. For this goal, researchers around the world have been trying to find ways to increase the yield of this crop. Optimization of fertilization [2,3,4], the introduction of improved wheat varieties [5], adoption and design of the appropriate crop rotation systems [6,7], and the mitigation of biotic factors effects (e.g., weeds and fungi) by applying appropriate management methods [8,9,10], can all contribute to this never-ending effort. Among biotic factors, weed infestation is bound to happen in open field crops and, consequently, it is essential to deal with this issue. Broadleaf and grass weeds create a lot of problems in cereal cultivations since they compete with them for nutrients, water, and light, which can lead to huge yield losses [11,12,13]. Among the numerous weed species that can be found in wheat cropping systems, littleseed canarygrass (Phalaris minor Retz.) [14], wild oat (Avena fatua L.) [15], wild mustard (Sinapis arvensis L.) [16], false cleavers (Galium spurium L.) [17], and catchweed (Galium aparine L.) [18] are some commonly found weeds that exhibit a highly competitive ability. Several herbicides alone or in mixtures are used to control both grass and broadleaf weeds in wheat crops [19].
In the last decades, herbicides belonging to the classes of sulfonylureas (e.g., metsulfuron-methyl, bensulfuron-methyl, and tribenuron-methyl) and triazolopyrimidines (e.g., florasulam and pyroxsulam) have been widely applied in cereal fields to minimize the yield loss from weed infestations. Both classes, according to the Herbicide Resistance Action Committee (HRAC), belong to group 2 based on their modes of action [20]. The herbicides of the abovementioned classes are inhibitors of the acetolactate synthase enzyme (ALS) that lead to a disruption of the biosynthesis of amino acids (valine, leucine, and isoleucine) causing plant death [21]. However, ALS inhibitors are among the herbicides with the most cases of resistant weeds compared to other herbicides with a different mode of action [22,23]. The main reasons for the extensive development of resistance to these classes of herbicides are their widespread usage and repeated application in the same field instead of applying herbicides with a different mode of action [23,24]. Other herbicides applied in cereal crops are aminopyralid and halauxifen-methyl (pyridine-carboxylates) as well as 2,4-D and MCPA (phenoxy-carboxylates). These herbicides are synthetic auxins that belong to group 4 based on their modes of action [20] and mimic auxin indole-3-acetic acid (IAA), causing growth abnormalities (e.g., deformation and epinasty) in the targeted plants [25,26,27,28]. Moreover, bromoxynil, an herbicide that belongs to the nitriles chemical class, is also applied in cereals. This herbicide is classified to group 6 based on its mode of action [20] and inhibits the electron transport from QA to QB in photosystem II (PSII), while plant death is due to cell membrane damage caused by lipid peroxidation [29,30]. The aforementioned herbicides, as well as other herbicides, can be used to control weeds in cereal crops. However, farmers should be aware of the risk of developing resistant weed populations in their fields, and, therefore, it is important to select and apply herbicides with a different mode of action year on year to minimize the selection pressure.
Galium spurium and G. aparine are broadleaf annual weeds of the Rubiaceae family [31] that are very competitive in cereal crops, which causes significant yield losses, while these weeds also make harvesting difficult since they can cause stem lodging [31,32]. These Galium species are widely spread around the world (e.g., Canada, China, Greece, Turkey, and Spain) under various environmental conditions, causing problems to cereals production, and their control is based on the application of herbicides [18,31,33,34,35]. In recent years, G. spurium herbicide resistance has been on the rise, making its control in some cereal fields difficult. Several populations of G. spurium have developed resistance to various groups of herbicides such as ALS inhibitors [e.g., chlorsulfuron, tribenuron-methyl, thifensulfuron-methyl/tribenuron-methyl, and triasulfuron (sulfonylureas), florasulam (triazolopyrimidines)] [32,33,36] and auxin mimic/cellulose biosynthesis-inhibiting herbicides (quinclorac (quinoline-carboxylates)) [32,37]. The aforementioned studies show that populations of G. spurium with resistance to herbicides are increasing and, consequently, the management of these resistant populations by applying effective herbicides is of great importance to maximize the wheat yield. Thus, this study aimed to evaluate (a) the efficacy of several post-emergence herbicides belonging to chemical classes with a different mode of action against a G. spurium population resistant to ALS-inhibiting herbicides, and (b) the effects of the resistant population on the growth and yield of durum wheat (Triticum durum Desf.). Finally, emphasis was given to the efficacy of halauxifen-methyl since this herbicide has been registered recently for use in wheat crops in several European countries.

2. Materials and Methods

2.1. Experimental Design and Main Cultural Practices

2.1.1. Site 1: Domokos

The first experiment was set at Domokos (39.0377 N, 22.3365 E; altitude: 492 m), in the region of Central Greece, from November 2021 to June 2022. The province of Domokos was chosen for the establishment of the field experiment because false cleavers is one of the most important weeds in cereals in this region. The Simeto variety of durum wheat was chosen for this experiment as it is a variety commonly cultivated in Greece. Wheat sowing was performed mechanically using a seeding cereal machine on 15 November 2021. The weather conditions throughout the cultivation period are presented in Figure 1, while the soil was clay in texture (sand: 25.7%, silt: 23.1%, and clay: 51.2%) with a pH of 7.6. The experimental design was a complete randomized block design with seven treatments and three replications for each treatment. The treatments were the following: C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl (Phyton), H2: pyroxsulam + cloquintocet-mexyl (safener) (Senior 75 WG)/florasulam + 2,4-D 2-ethylhexyl ester (EHE) (Titanas SE), H3: aminopyralid + florasulam (Lancelot 450 WG), H4: 2,4-D 2-EHE + bromoxynil (Brominal Nuevo), and H5: halauxifen-methyl + florasulam + cloquintocet-mexyl (safener) (Quelex). Each plot was 6 m2 (2 m × 3 m) and the wheat cultivar was sown at 280 kg ha−1 (row spacing: 18 cm) at a depth of 3 to 5 cm. Conventional basic NPK fertilizer 16-20-0 was applied at sowing (300 kg ha−1), while at the tillering stage, top-dressing fertilization was performed using calcium ammonium nitrate at the rate of 300 kg ha−1. In the field where the experiment was carried out, the population of false cleavers was resistant to sulfonylureas and triazolopyrimidines herbicides. The resistance of this false cleavers population to herbicides tribenuron-methyl, mesosulfuron-methyl + iodosulfuron-methyl-sodium, and florasulam + 2,4-D was previously confirmed in a pot trial. In that preliminary trial conducted from December 2020 to April 2021, the aforementioned herbicides were applied at the recommended doses (x) and four times the recommended doses (4x) to this population as well as on a susceptible population that was collected from the same region for the validation of resistance.

2.1.2. Site 2: Velestino

The second experiment was set at Velestino (39.3959 N, 22.7568 E; altitude: 76 m), in the region of Thessaly, from November 2021 to June 2022. The same variety (Simeto) of durum wheat was chosen for this experiment as well for consistency. Sowing was performed mechanically using a cereal seed machine on 11 November 2021. Before sowing with wheat, the population of false cleavers with resistance to ALS-inhibiting herbicides was hand sown. For false cleavers sowing, a mixture (8.75 g) of seeds and plant debris containing about 2500 seeds was spread uniformly on each plot. It is important to highlight that there was no natural population of false cleavers in the experimental field. The seeds of false cleavers were collected in the middle of June 2021 from plants grown on the same field of site 1 in a durum wheat crop. The weather conditions throughout the wheat’s growth are presented in Figure 1. The soil was classified as sandy clay loam (sand: 38%, silt: 36%, and clay: 26%) and had a pH value of 7.4. The experimental design was a complete randomized block design with five treatments with three replications for each treatment. The treatments were the following: C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H4: 2,4-D 2-ethylhexyl ester (EHE) + bromoxynil, and H5: halauxifen-methyl + florasulam + cloquintocet-mexyl (safener). Each plot was 7.5 m2 (2.5 m × 3 m), and the wheat cultivar was sown at 250 kg ha−1 at a depth of 3 to 5 cm. The row spacing was 18 cm. The same fertilization schedule was performed in this experimental site as well.

2.2. Herbicides Application and Doses

At both sites, all herbicides were applied at their maximum recommended doses: H1: metsulfuron-methyl (4 g a.i. (active ingredient) ha−1) + bensulfuron-methyl (50 g a.i. ha−1), H2: pyroxsulam (18.75 g a.i. ha−1) + cloquintocet-mexyl (safener)/florasulam (4.725 g a.i. ha−1) + 2,4-D 2-EHE (339.375 g a.i. ha−1), H3: aminopyralid (9.9 g a.i. ha−1) + florasulam (4.95 g a.i. ha−1), H4: 2,4-D 2-EHE (633.15 g a.i. ha−1) + bromoxynil (octanoate/heptanoate ester, 601.2 g a.i. ha−1), and H5: halauxifen-methyl (5.6 g a.i. ha−1) + florasulam (5.155 g a.i. ha−1) + cloquintocet-mexyl (safener). Herbicides H1, H2, H3, and H5 were tank mixed with the adjuvant alkylphenol alkoxylate (99% w/v) at 200 mL per 100 L of spray solution. The herbicides were applied with a handheld field plot sprayer (boom width of 2 m with flat fan nozzles, spray volume: 300 L ha−1, pressure: 2.5 atm) at the end of tillering and beginning of stem elongation (BBCH growth stages 30 and 31) to provide thorough coverage and a uniform spray pattern. This application was conducted on 7 April 2022 and 16 March 2022 at Site 1 (Domokos) and Site 2 (Velestino), respectively. In the weed-free plots, all of the weeds were controlled by hand hoeing one day before herbicide application on 6 April 2022 and 15 March 2022, at Domokos and Velestino, respectively.

2.3. Sampling and Measurements

The dry above-ground biomass measurement of wheat was conducted for each experimental site performing destructive measurements by cutting plants in an area of 0.36 m2 in each plot. The samples were oven-dried at 60 °C for four days. For the measurements of stem height and spike length, five plants were randomly selected from each plot. These parameters were measured on the main stem of the plants. Moreover, for the determination of chlorophyll content, a portable chlorophyll meter (model SPAD-502, Konica Minolta, Optics, Inc., Osaka, Japan) was used in the field by randomly selecting five plants from each treatment. The SPAD values were measured on the flag leaves in the middle of the blades. The abovementioned parameters were measured on 9 May 2022 and 19 May 2022 at Velestino (Site 2) and Domokos (Site 1), respectively. Durum wheat crops were harvested on the second fortnight of June, while after the harvest, the 1000-seed weight (three samples of 100 seeds) and the yield per hectare were calculated for each treatment. At the Domokos site, the durum wheat crop was hand harvested on an area of 1 m2, while at Velestino, the harvest was conducted mechanically (harvest width 1.4 m) on an area of 3.5 m2 (2.5 m × 1.4 m).
With regards to weed measurements, the dry biomass of false cleavers and other weed species was measured after drying at 60 °C for four days. Sampling was conducted on 9 May 2022 and 19 May 2022 at Velestino and Domokos, respectively, using a square quadrate (0.6 m × 0.6 m), which was randomly placed in the center of each plot. Finally, the herbicide efficacy (%) against false cleavers was determined based on its dry biomass data.

2.4. Statistical Analysis

To evaluate the effects of the applied herbicides on both durum wheat and weed parameters, an analysis of variance (ANOVA) was conducted according to the randomized complete block design using IBM SPSS software ver. 24 (IBM Corp., Armonk, NY, USA). Mean comparisons were made using Duncan’s multiple range test (p ≤ 0.05), while Pearson’s correlation analysis (Table 1) was performed to assess the relationships among the evaluated parameters. SigmaPlot 12 software (Systat Software, Inc., Palo Alto, NC, USA) was used for making the figures in this manuscript.

3. Results

3.1. Weather Conditions

At the Velestino site, the total precipitation during the growing period between November to June was about 370 mm, while at Domokos, the precipitation was higher than 600 mm. Moreover, the mean monthly temperatures during the growing period were lower at Domokos compared to those at Velestino. It is also important to highlight that the mean temperature in March was lower than that in February, while the reverse is usually observed.

3.2. Weeds Dry Biomass

The dry biomass of false cleavers presented statistically significant differences among the treatments (Figure 2). At Domokos, the false cleavers dry biomass was higher in the metsulfuron-methyl + bensulfuron-methyl and pyroxsulam/florasulam + 2,4-D (>1000 kg ha−1) treatments without a statistically significant difference with the untreated control, as a result of the resistance of false cleavers to the aforementioned herbicides belonging to sulfonylureas and triazolopyrimidines.
False cleavers biomass was significantly decreased in the other herbicide applications. More specifically, aminopyralid + florasulam had the highest biomass followed by bromoxynil + 2,4-D and halauxifen-methyl + florasulam, which exhibited the highest false cleavers control among them. At Velestino, bromoxynil + 2,4-D and halauxifen-methyl + florasulam provided greater efficacy (>95%) against false cleavers (Figure 3), exhibiting a dry biomass of 23.8 and 20.7 kg ha−1, respectively, whereas the false cleavers population was highly resistant to metsulfuron-methyl + bensulfuron-methyl since the efficacy of this herbicide was 10.6%.
At the Domokos site, apart from the false cleavers, the dominant weeds were Sinapis arvensis L. and Veronica persica L., while the species Anthemis arvenis L., Lamium amplexicaule L., Avena sterilis L., Papaver rhoeas L., Fumaria officinalis L., Sonchus oleraceus L., Helminthotheca echioides (L.) Holub, and Geranium dissectum L. were recorded at lower densities. In the untreated control, the false cleavers density on 19 May was 13 plants m−2, while the density of other weed species was 27.1 plants m−2. Similarly, at Velestino, apart from the false cleavers, the dominant weeds were S. arvensis, A. arvensis, L. amplexicaule, and P. rhoeas, while V. persica, S. oleraceus, and F. officinalis were observed at lower densities. In the untreated control, the false cleavers density on 9 May was 40.7 plants m−2, while the density of other weed species was 14.0 plants m−2.
Considering the total dry biomass of weeds (Figure 4), bromoxynil + 2,4-D and halauxifen-methyl + florasulam applications presented the lowest values among herbicide treatments, with statistically significant differences and values close to the weed-free treatment. The total dry biomass of weeds in the plots where metsulfuron-methyl + bensulfuron-methyl were applied was 1073 kg ha−1 and 1598 kg ha−1 at Velestino and Domokos, respectively, which were values that were 2.1 to 2.7-fold lower compared to the untreated control.

3.3. Relative Chlorophyll Content

The relative chlorophyll content (SPAD values) in the leaves of durum wheat presented statistically significant differences among the treatments (Figure 5). At the Domokos site, the highest chlorophyll content (51.5 to 53.1 SPAD values) was found with the halauxifen-methyl + florasulam, bromoxynil + 2,4-D, and aminopyralid + florasulam herbicides, while there were no statistically significant differences between them and the weed-free treatment (52.2 SPAD value). In the plots where pyroxsulam/florasulam + 2,4-D herbicide was applied, the chlorophyll contents of the leaves were the lowest, and the values were even lower in the metsulfuron-methyl + bensulfuron-methyl treatment group. The latter herbicide did not differ statistically significantly in this parameter with the untreated control (45.5 SPAD value). At Velestino, on the other hand, in treatments where the weeds were effectively controlled (bromoxynil + 2,4-D, halauxifen-methyl + florasulam, and weed-free control), the chlorophyll content was statistically significantly higher than the untreated control.

3.4. Durum Wheat Growth

The statistical analysis of wheat’s growth characteristic measurements showed that height was affected by the herbicide treatments only at Domokos (Figure 6). In contrast, plant biomass showed statistically significant differences at both experimental sites.
More specifically, at Domokos, the stem height of the plants in the herbicide treatments ranged from 79.6 cm to 81.7 cm with no statistically significant differences among them, but there were statistically significant differences between them and the untreated control (75.4 cm). At Velestino, in all treatments, this parameter ranged from 76.6 cm to 79.6 cm. In the case of dry biomass (Figure 7), at Domokos, the greatest biomass values (8508 to 8923 kg ha−1) were found in plots where the herbicides bromoxynil + 2,4-D, halauxifen-methyl + florasulam, and aminopyralid + florasulam were applied, with no statistically significant differences between them and the weed-free treatment (8758 kg ha−1). In the pyroxsulam/florasulam + 2,4-D and metsulfuron-methyl + bensulfuron-methyl plots, significantly and statistically lower values of dry biomass (7490 and 7203 kg ha−1, respectively) were recorded compared to the other herbicides. At Velestino, the weed-free control, bromoxynil + 2,4-D, and halauxifen-methyl + florasulam treatments presented significantly higher values of plant biomass (>13,000 kg ha−1) compared to that in the metsulfuron-methyl + bensulfuron-methyl and the untreated control treatments (<12,000 kg/ha), which did not statistically differ between them.

3.5. Spike Length, 1000-Seed Weight, and Seed Yield

Herbicide treatments had no statistically significant impact on the spike length (Figure 8); however, the 1000-seed weight and yield of the durum wheat in both experimental sites (Figure 9 and Figure 10) were affected statistically significantly. More specifically, spike length ranged from 6.1 cm to 6.6 cm and from 6.2 cm and 6.5 cm at Domokos and Velestino, respectively.
Regarding the 1000-seed weight (Figure 9), at Domokos, bromoxynil + 2,4-D and halauxifen-methyl + florasulam applications presented the highest values of 1000-seed weight followed by the weed-free control and aminopyralid + florasulam. Significantly lower 1000-seed weights (50.8 to 51.1 g) were recorded for the wheat seeds in the treatments where pyroxsulam/florasulam + 2,4-D and aminopyralid + florasulam were applied, while the lowest 1000-seed weight was recorded in the untreated control (48.5 g). At Velestino, the greatest values of 1000-seed weight (≥53.5 g) were observed with bromoxynil + 2,4-D, halauxifen-methyl + florasulam, and weed-free treatments.
In the case of seed yield (Figure 10), at Domokos, the highest performing treatments were the bromoxynil + 2,4-D, halauxifen-methyl + florasulam, and the weed-free control (>3500 kg/ha, respectively), followed by aminopyralid + florasulam (3332 kg ha−1). Among the herbicides that were applied, the lowest seed yield was presented with the pyroxsulam/florasulam + 2,4-D and metsulfuron-methyl + bensulfuron-methyl (<3000 kg/ha) treatments, which was significantly higher than the untreated control (2204 kg ha−1). At Velestino, the highest seed yield was observed at the weed-free treatment (4644 kg ha−1) followed by halauxifen-methyl + florasulam (4564 kg ha−1) and bromoxynil + 2,4-D (4525 kg ha−1) without statistically significant differences between them. In contrast, the lowest seed yield was observed in the untreated control and the metsulfuron-methyl + bensulfuron-methyl treatment groups (<4200 kg ha−1). The decrease in seed yield between the untreated control and other treatments was up to 39.4% and 13.8% at Domokos and Velestino, respectively.

4. Discussion

False cleavers control has been a troubling issue over the last years in crop production as several populations of this species have been found resistant to sulfonylureas, triazolopyrimidines, and auxin mimic groups of herbicides [32,33,37]. In our experiments, the herbicides metsulfuron-methyl + bensulfuron-methyl (ALS-inhibiting herbicides) and pyroxsulam/florasulam + 2,4-D (a combination of ALS inhibitors with auxin-mimic herbicide) slightly inhibited the growth of false cleavers without causing plant necrosis (Figure 11b). The aforementioned herbicides caused a lower than 11% reduction in the dry biomass of false cleavers compared to the untreated control. This result is in agreement with other research studies that claimed that some false cleavers populations are resistant to ALS-inhibiting herbicides. In the field, at the Domokos site, herbicides that belonged to sulfonylureas and triazolopyrimidines groups had been applied for at least 10 years of the previous 25 years. However, it should be noted that the herbicides that could not control false cleavers in our experiments had adequate efficacy against the rest of the broadleaved weeds in the field. In a pot experiment, Papapanagiotou et al. [33] found that several populations of false cleavers in the northern region of Greece were highly resistant to chlorsulfuron and tribenuron-methyl and were not controlled, even when doses much higher (e.g., 8x) than the recommended field dose (x) were applied, while three of these populations (e.g., GS 1 Kitros and GS 6 Kolindros) exhibited cross-resistance to florasulam + 2,4-D. In Canada, according to Beckie et al. [38], resistant populations of false cleavers to ALS-inhibiting herbicides are steadily occurring in various regions (e.g., Alberta and Saskatchewan), while Hall et al. [32] reported that a false cleavers population originating from Central Alberta exhibited multiple resistance to sulfonylureas herbicides (triasulfuron and thifensulfuron + tribenuron) and quinclorac.
Regarding the efficacy of the other herbicides against false cleavers, our results indicated that florasulam + aminopyralid provided low efficacy (57%) against this weed species. In contrast, Papapanagiotou et al. [33] reported that florasulam + aminopyralid, florasulam + fluroxypyr, and tribenuron-methyl + mecoprop-p were highly effective (100%) against the false cleavers populations resistant to sulfonylureas tribenuron-methyl and chlorsulfuron. In another study, Hall et al. [32] observed that the population of this species resistant to sulfonylureas was susceptible to both fluroxypyr and MCPA + mecoprop + dicamba. Moreover, the results of the current study revealed that the most effective herbicides against false cleavers were bromoxynil + 2,4-D and halauxifen-methyl + florasulam. The efficacy of bromoxynil + 2,4-D was 73% and 97% (Figure 11c) at Domokos and Velestino, respectively, while the halauxifen-methyl + florasulam efficacy ranged between 89% and 97% (Figure 11e,f). It is important to point out that the latter herbicide was recently registered (autumn of 2021) in Greece for use in various cereal crops including durum wheat, barley (Hordeum vulgare L.), and rye (Secale cereale L.). In another study, halauxifen-methyl has been proven to be effective (99%) against a Canada fleabane (Erigeron canadensis L.) population with resistance to glyphosate [39]. However, since it is a relatively new herbicide, more research should be carried out to examine its efficacy against weed species with resistance to other herbicides that belong to the auxin mimics group, sulfonylureas, and triazolopyrimidines. The mistakes of the past in chemical weed control should be avoided for recently discovered herbicides. Thus, halauxifen-methyl + florasulam rotation with herbicides of a different mode of action must be implemented by farmers to prevent the development of resistant false cleavers populations to this newly registered herbicide.
Competition between wheat crops and broadleaf and/or grass weed species such as wild oat, milk thistle (Silybum marianum (L.) Gaertn.), and wild mustard can cause a significant reduction in seed yield, and, thus, the herbicide application is imperative to maximize crop production [13,15,16]. The proper selection of an herbicide is important to maximize seed yield in wheat cultivation and depends mainly on the weed species that prevail in a field. The development of resistant weed populations in a field is also a significant parameter that must be taken into account when choosing an herbicide. In both experimental sites, the herbicides that were applied reduced weed biomass and contributed to the improved growth of durum wheat plants and increased seed production. The results of the correlation analysis (Table 1) indicated that there was a negative and significant correlation between total weed biomass and various crop parameters such as durum wheat dry biomass (r = −0.862, p = 0.001 and r = −0.829, p = 0.001, at Domokos and Velestino, respectively) and seed yield (r = −0.910, p = 0.001 and r = −0.814, p = 0.001, at Domokos and Velestino, respectively). It is also important to point out that the increase in crop yield was greater in the herbicides that effectively controlled the resistant population of false cleavers, indicating the highly competitive ability of this weed species. This result is confirmed by the correlation analysis since there was a negative and significant correlation between false cleavers dry biomass and durum wheat dry biomass (r = −0.828, p = 0.001 and r = −0.812, p = 0.001, at Domokos and Velestino, respectively) as well as seed yield (r = −0.881, p = 0.001 and r = −0.809, p = 0.001, at Domokos and Velestino, respectively). For example, the herbicides bromoxynil + 2,4-D and halauxifen-methyl + florasulam increased seed yield by up to 39.4% compared to the untreated control. Similar results were observed by Karkanis et al. [16] who found that effective control of wild mustard and milk thistle caused an increase in the seed yield of durum wheat crops by up to 42.8% compared to the untreated control. In another study, Wolf et al. [40] reported that the herbicide bromoxynil + MCPA effectively controlled a kochia (Bassia scoparia (L.) A. J. Scott) population with resistance to ALS-inhibiting herbicides (thifensulfuron + tribenuron), which resulted in increased wheat productivity.
Regarding phytotoxicity symptoms, slight chlorosis was observed only with the use of the pyroxsulam/florasulam +2,4-D herbicide. However, these symptoms were transient and did not have an impact on the plant’s growth. In another study, bromoxynil + 2,4-D, when applied in a mixture with the fungicides azoxystrobin or trifloxystrobin + prothioconazole that belong to strobilurins and triazoles groups, caused a slight injury (<5.5%) on wheat leaves only when low temperatures prevailed 2 to 5 days after application [41]. In field experiments conducted in Mississippi and Oklahoma (USA) for two consecutive years 2018–2019 and 2019–2020, Ferguson et al. [42] observed that the herbicide halauxifen-methyl + florasulam did not cause phytotoxicity in a winter wheat (Triticum aestivum L.) crop and had no negative impact on crop yield. These findings are in agreement with our results in which halauxifen-methyl + florasulam application did not cause injury to durum wheat. It is also important to mention that durum wheat productivity was lower in Domokos compared to Velestino. In Domokos, the low temperatures during February and March, in combination with high precipitation levels, caused stress on durum wheat plants, delaying their growth and, consequently, resulting in a lower competitive ability against false cleavers and other broadleaf weeds. In the untreated control, the durum wheat dry biomass to false cleavers biomass ratio was approximately 5 and 13 in Domokos and Velestino, respectively. This result confirmed that the competitive ability of the crop against false cleavers was lower in Domokos compared to Velestino.

5. Conclusions

The results of our study show that the false cleavers population originating from the Domokos region was resistant to ALS-inhibiting herbicides (sulfonylureas and triazolopyrimidines). Even though the herbicides with the abovementioned mode of action did not control false cleavers, bromoxynil + 2,4-D and the newly implemented herbicide halauxifen-methyl + florasulam provided high control against this species at both experimental fields, contributing to increasing 1000-seed weights and yields in durum wheat crops. The efficacy of both herbicides was higher in Velestino than in Domokos because, at the latter site, false cleavers plants had greater growth at the time of application. Our findings confirm that the issue of the resistance of false cleavers against ALS-inhibiting herbicides such as sulfonylureas exists and other herbicides need to be implemented in weed management programs. Both herbicides bromoxynil + 2,4-D and halauxifen-methyl + florasulam seem to be a great addition to the integrated management of resistant false cleavers populations; however, more research needs to be carried out to have a variety of alternative herbicides that can contribute to the solution of this problem.

Author Contributions

Conceptualization, P.S., A.E. and A.K.; formal analysis, P.S., N.K. and A.K.; investigation, P.S.; methodology, A.E., N.K. and A.K.; supervision, A.K.; visualization, P.S. and A.E.; writing—original draft, P.S. and A.K.; writing—review and editing, A.E., N.K. and A.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The data presented in this study are available in this article.

Acknowledgments

The authors would like to thank Spyridon Souipas and Christos Karamoutis for their technical assistance in the experiment conducted at Velestino.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Weather conditions (mean air temperature and precipitation) throughout wheat’s growth period (November 2021 to June 2022) in both sites (Domokos and Velestino).
Figure 1. Weather conditions (mean air temperature and precipitation) throughout wheat’s growth period (November 2021 to June 2022) in both sites (Domokos and Velestino).
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Figure 2. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on false cleavers dry biomass (kg ha−1) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 111.567 *** (Site 1: Domokos) and F = 109.565 *** (Site 2: Velestino). *** significant at p < 0.001.
Figure 2. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on false cleavers dry biomass (kg ha−1) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 111.567 *** (Site 1: Domokos) and F = 109.565 *** (Site 2: Velestino). *** significant at p < 0.001.
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Figure 3. Efficacy of treatments (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) against false cleavers (%) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 366.854 *** (Site 1: Domokos) and F = 502.076 *** (Site 2: Velestino). *** significant at p < 0.001.
Figure 3. Efficacy of treatments (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) against false cleavers (%) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 366.854 *** (Site 1: Domokos) and F = 502.076 *** (Site 2: Velestino). *** significant at p < 0.001.
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Figure 4. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on total weed dry biomass (kg ha−1) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 179.729 ***(Site 1: Domokos) and F = 380.623 *** (Site 2: Velestino). *** significant at p < 0.001.
Figure 4. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on total weed dry biomass (kg ha−1) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 179.729 ***(Site 1: Domokos) and F = 380.623 *** (Site 2: Velestino). *** significant at p < 0.001.
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Figure 5. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on relative chlorophyll content (SPAD values) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 26.474 *** (Site 1: Domokos) and F = 11.126 ** (Site 2: Velestino). ** and *** significant at p < 0.01 and p < 0.001.
Figure 5. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on relative chlorophyll content (SPAD values) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 26.474 *** (Site 1: Domokos) and F = 11.126 ** (Site 2: Velestino). ** and *** significant at p < 0.01 and p < 0.001.
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Figure 6. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on stem height (cm) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 10.100 *** (Site 1: Domokos) and F = 1.972 ns (Site 2: Velestino). *** significant at p < 0.001. ns = not significant.
Figure 6. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on stem height (cm) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 10.100 *** (Site 1: Domokos) and F = 1.972 ns (Site 2: Velestino). *** significant at p < 0.001. ns = not significant.
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Figure 7. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on dry weight (kg ha−1) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOA: F = 11.354 *** (Site 1: Domokos) and F = 10.114 ** (Site 2: Velestino). ** and *** significant at p < 0.01 and p < 0.001.
Figure 7. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on dry weight (kg ha−1) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOA: F = 11.354 *** (Site 1: Domokos) and F = 10.114 ** (Site 2: Velestino). ** and *** significant at p < 0.01 and p < 0.001.
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Figure 8. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on spike length (cm) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 0.749 ns (Site 1: Domokos) and F = 0.664 ns (Site 2: Velestino). ns = not significant.
Figure 8. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on spike length (cm) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 0.749 ns (Site 1: Domokos) and F = 0.664 ns (Site 2: Velestino). ns = not significant.
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Figure 9. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on 1000-seed weight (g) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 12.944 *** (Site 1: Domokos) and F= 7.262 ** (Site 2: Velestino). ** and *** significant at p < 0.01 and p < 0.001.
Figure 9. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on 1000-seed weight (g) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 12.944 *** (Site 1: Domokos) and F= 7.262 ** (Site 2: Velestino). ** and *** significant at p < 0.01 and p < 0.001.
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Figure 10. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on seed yield (kg ha−1) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 22.340 *** (Site 1: Domokos) and F = 9.156 ** (Site 2: Velestino). ** and *** significant at p < 0.01 and p < 0.001.
Figure 10. Herbicide treatment (C1: untreated control, C2: weed-free control, H1: metsulfuron-methyl + bensulfuron-methyl, H2: pyroxsulam/florasulam + 2,4-D, H3: aminopyralid + florasulam, H4: bromoxynil + 2,4-D, and H5: halauxifen-methyl + florasulam) effects on seed yield (kg ha−1) at two sites. Values are presented as means of three replicates ± standard deviation. Mean values followed by different letters have statistically significant differences according to Duncan’s multiple range test at p < 0.05. F values of ANOVA: F = 22.340 *** (Site 1: Domokos) and F = 9.156 ** (Site 2: Velestino). ** and *** significant at p < 0.01 and p < 0.001.
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Figure 11. (a) The experimental field in Velestino at 14 days after herbicides application (DAA), (b) false cleavers growth in the metsulfuron-methyl + bensulfuron-methyl plots at 14 DAA, (c) necrosis of false cleavers plants in bromoxynil + 2,4-D at 14 DAA, (d) false cleavers growth in the control plots in Domokos, (e) halauxifen-methyl + florasulam symptoms on false cleavers plants at 14 DAA, and (f) false cleavers necrosis in the halauxifen-methyl + florasulam treatment.
Figure 11. (a) The experimental field in Velestino at 14 days after herbicides application (DAA), (b) false cleavers growth in the metsulfuron-methyl + bensulfuron-methyl plots at 14 DAA, (c) necrosis of false cleavers plants in bromoxynil + 2,4-D at 14 DAA, (d) false cleavers growth in the control plots in Domokos, (e) halauxifen-methyl + florasulam symptoms on false cleavers plants at 14 DAA, and (f) false cleavers necrosis in the halauxifen-methyl + florasulam treatment.
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Table
Table 1. Pearson’s correlation coefficients (r) for plant height (PH), durum wheat dry biomass (WhDB), relative chlorophyll content (SPAD), 1000-seed weight (SW), spike length (SL), seed yield (SY), false cleavers dry biomass (GDB), and total weed dry biomass (WeDB).
Table 1. Pearson’s correlation coefficients (r) for plant height (PH), durum wheat dry biomass (WhDB), relative chlorophyll content (SPAD), 1000-seed weight (SW), spike length (SL), seed yield (SY), false cleavers dry biomass (GDB), and total weed dry biomass (WeDB).
Site 1: DomokosSHWhDBSPADSWSLSYGDBWeDB
SH10.770 ***0.705 ***0.818 ***0.1320.794 ***−0.639 **−0.843 ***
WhDB–10.889 ***0.870 ***0.1580.870 ***−0.828 ***−0.862 ***
SPAD––10.827 ***0.0720.891 ***−0.888 ***−0.864 ***
SW–––10.2130.835 ***−0.727 ***−0.852 ***
SL––––10.183−0.313−0.075
SY–––––1−0.881 ***−0.910 ***
GDB––––––10.841 ***
WeDB–––––––1
Site 2: VelestinoSHWhDBSPADSWSLSYGDBWeDB
SH10.4360.517 *0.0330.4230.258−0.326−0.350
WhDB–10.587 *0.711 **0.1520.901 ***−0.812 ***−0.829 ***
SPAD––10.3960.3300.542 *−0.688 ***−0.817 ***
SW–––1−0.1420.694 *−0.850 ***−0.653 **
SL––––10.098−0.177−0.058
SY–––––1−0.809 ***−0.814 ***
GDB––––––10.875 ***
WeDB–––––––1
*, **, and *** significant at p = 0.05, 0.01, and 0.001 (two-tailed test of significance), respectively. N = 21 and 15 for site 1 (Domokos) and site 2 (Velestino), respectively.
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Sparangis, P.; Efthimiadou, A.; Katsenios, N.; Karkanis, A. Control of Resistant False Cleavers (Galium spurium L.) Population to ALS-Inhibiting Herbicides and Its Impact on the Growth and Yield of Durum Wheat. Agronomy 2023, 13, 1087. https://doi.org/10.3390/agronomy13041087

AMA Style

Sparangis P, Efthimiadou A, Katsenios N, Karkanis A. Control of Resistant False Cleavers (Galium spurium L.) Population to ALS-Inhibiting Herbicides and Its Impact on the Growth and Yield of Durum Wheat. Agronomy. 2023; 13(4):1087. https://doi.org/10.3390/agronomy13041087

Chicago/Turabian Style

Sparangis, Panagiotis, Aspasia Efthimiadou, Nikolaos Katsenios, and Anestis Karkanis. 2023. "Control of Resistant False Cleavers (Galium spurium L.) Population to ALS-Inhibiting Herbicides and Its Impact on the Growth and Yield of Durum Wheat" Agronomy 13, no. 4: 1087. https://doi.org/10.3390/agronomy13041087

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