Introduction
Every year a major threat to agricultural production comes from the infestations with wild plant species (weeds). Since the dawn of agriculture, human beings have battled against weeds to improve crop survival and productivity. Weeds have an adverse impact on agricultural production and represent the most significant pest threat to crop yields. Weeds are unanimously considered one of the costliest and limiting factors in crop production. Crop yield reductions caused by weeds are mainly derived from direct competition with crop plants for available water, nutrients, light, and space, which causes great losses (Rosskopf et al., 1999).
The physiological and biochemical processes of weeds can be disrupted by herbicides, especially through a specific interaction with a single target molecule in a plant. At the appropriate concentration, herbicide molecules are transmitted into the target cells of a plant, which inhibit vascular processes so that the plant can no longer continue to survive (Devine and Preston, 2000). Recently, modern herbicides have largely replaced human, animal, and mechanical weed controls. They have made a great contribution to the high productivity of worldwide agriculture (Powles and Yu, 2010).
Herbicide resistance in weeds is not a new phenomenon but is somewhat less known and experienced than insecticide or fungicide resistance. According to the definition given by the Weed Science Society of America (WSSA), herbicide resistance refers to a species or a plant surviving and reproducing by its intrinsic natural ability after herbicide treatment without any selection or genetic dominant. Selection of resistant biotypes may result in control failures. Therefore, selection pressure is an essential requirement for herbicide resistance.
The first report of herbicide resistance was around the 1960s with the finding of triazine resistant common groundsel and 2,4-D resistant bindweed. Since that time, a total of 216 weed biotypes around the world have evolved resistance to herbicides (Ryan, 1970; Vargas, 2001). In an agricultural situation, herbicide resistance is the evolved ability for an herbicide susceptible weed population to withstand and complete its life cycle after an herbicide has been applied at its normal rate.
History of herbicide resistance
Herbicides are applied to the soil to manage weeds. It is necessary to control weeds during the crop growing season, but it is not desirable for herbicides to persist and affect the following crop growth. Moreover, herbicides can provide impressive levels of weed control in many crop and non-crop situations. However, not all weedy species are equally controlled due to the varying levels of natural tolerance or evolution of herbicide-resistant weed biotypes which is a result of the repeated use of the same herbicides or herbicides with the same modes of action imposing a great degree of selection pressure on weed populations (Hanson et al., 2013).
Beginning in the 1980s, the number of reported resistant biotypes began rapidly increasing in the United State and worldwide. Since then, resistance to one or more of the 25 herbicide families has been observed in more than 65 weed species in the U.S (Shaner, 2014).
Some modes of action have been a greater problem in herbicide resistance than others (Bo et al., 2017). For instance, the greatest number of resistant biotypes worldwide has been observed with acetolactate synthase (ALS)-inhibitors (imidazolinones, pyrimidinylthiobenzoates, sulfonylureas, and triazolopyrimidines). Over the past decade, the most important area of herbicide chemistry has been the discovery of herbicides that inhibit ALS. ALS catalyzes the formation of the essential amino acids valine, leucine, and isoleucine, all of which are necessary for protein formation and subsequent plant development (Heap, 1997). Nowadays, the evolved resistance of weeds to the mode of action of this herbicide has resulted in the selection for resistant biotypes in 160 weed species (98 dicots and 62 monocots) (Heap, 2018).
Over the last three decades, increasing resistant biotypes to other modes of action of herbicides have been reported. In 1978, herbicides inhibiting the activity of Acetyl-CoA carboxylase (ACCase), a key enzyme that regulates the metabolism of fatty acids in monocotyledonous plants, made their first appearance on the market. Only four years later, in 1982, resistance to ACCase inhibitors was reported in Australia. Today, 48 weed species (monocots only) worldwide have evolved resistance to this group of herbicides (Heap, 2017).
The second most common herbicide with resistant biotypes is the photosystem II inhibitors (primarily triazines). Cases reporting resistance to PSII-inhibitors have been documented in several weed species including Capsella bursa-pastoris L., Chenopodium album L., Setaria viridis L., Echinochloa crus-galli L., and Alopecurus myosuroides Huds. (Grignac, 1978). Resistance to PSII-inhibitors occurred because of the repetitive use and high residual activity of these compounds which consequently resulted in selection pressure for resistant biotypes. Up till now, 74 weed species (51 dicots and 23 monocots) have been identified to have evolved resistance to PSII-inhibitors in the world (Heap, 2018).
Glyphosate is used as a board spectrum herbicide for crops after both the crop and weeds have emerged. There is no chemical that has had a greater positive impact on weed management than the herbicide glyphosate. In fact, glyphosate is widely used worldwide. Glyphosate inhibition of the 5-enolpyruvyl-shikimate synthase (EPSPS) activity disrupts the shikimate pathway and inhibits aromatic amino acid production which is vital for protein synthesis in plant growth (Dill, 2005). Therefore, glyphosate was less toxic than some of the other pesticides available and enabled more farmers to adopt a no-tillage approach, both of which were better for the environment. Glyphosate was introduced to the world by the Monsanto Company in 1974. Currently, 43 weed species (23 dicots and 20 monocots) worldwide have evolved resistance to this group of herbicides (Heap, 2018).
Scientists have said that ten specific weed species were confirmed to be especially hard to kill. Most farmers are raising awareness of the fact that they are finding the most important herbicide resistant species of weeds difficult to control as they become resistant to the most popular herbicides (Table 1).
Recently, the reliance on modern herbicides has been increasing which has led to a reduction in the need of traditional techniques for weed control. However, the application of herbicides to large weed communities induces a high rate of genetic diversity which causes a strong selection pressure promoting resistance evolution (Fig. 1 and 2).
Today, globally, there are 255 herbicide-resistant weeds species (148 dicots and 107 monocots). Weeds have evolved resistance to 23 of the 26 known herbicide sites of action and to 163 different herbicides. Herbicide resistant weeds have been reported in 92 crops in 70 countries globally (Heap, 2018).
Herbicide resistance in Korea
Agriculture is also an important sector of the . Natural resources for agriculture in South Korea are not abundant. The arable land occupies only 22 percent of the area of the country, and two-third of the country is occupied by mountains and hills. A total of 28 families and 90 species of weeds occurred in the rice fields of Korea (Lee et al., 2017a). The weeds occur in the descending order of Echinochloa spp, Monochoria vaginalis and Schoenoplectus juncoides although there are differences according to climate and area (Lee et al., 2017b).
The total area under rice cultivation in Korea has been found to be 746,614 ha, out of which 20.9% of that area is infested by herbicide-resistant weeds which is 167.081 ha (Park et al., 2011b). In a 2011 survey, the areas infested with herbicide-resistant weeds in Chungnam, Jeonbuk and Jeonnam provinces were 72,736 ha (47.6%), 35,194 ha (16.4%) and 21,410 ha (36.9%), respectively (Lee et al., 2012). In a 2017 survey, in the Chungnam province, the infested area with a herbicide-resistant weed was 64,782 ha (47.0%). However, these areas in the Jeonbuk and Jeonnam provinces increased to 81,494 ha (68.9%) and 91,543 ha (51.5%), respectively, and the incidence of herbicide-resistant weeds has increased in other provinces (Jeong et al., 2018, Lee et al., 2018a, Lee et al., 2018b, Won et al., 2018). Recently, the occurrence of resistant weeds has increased in new areas (Won et al., 2018). This shows that the increase rate of herbicide resistant weed areas was considerably, and if this pace continues, we expect many more infested areas in the coming future.
In Korea, rice cultivation areas have decreased by 16 percent from 1995 to 2010; however, herbicide use has increased. The percentage of herbicide use in rice cultivation areas increased by 116% in 1995 followed by an increase of 205% in 2010 (Park et al., 2011a). The rapid increase of herbicide use in rice cultivation areas is due to the development of resistant weeds to sulfonylurea (SU) herbicides which have been introduced since the late 1980s; furthermore, the continuous use of ACCase and ALS inhibitors has led to the selection of herbicide-resistant Echinochloa spp. in direct-seeded rice cultivation of Korea.
In the history of paddy herbicide use in Korea since 1989, SU herbicides have been widely used as a "One-shot" weed control. The applied areas of SU-containing herbicides have been increasing rapidly by 69 and 96%, respectively. This is because these herbicides have a broad control spectrum against sedges and broadleaved weeds (Park et al., 2014). Additionally, they are major components of many commercial herbicides used for rice production. The extensive and persistent use of these herbicides with a relatively long residual activity and high selection for the last ten years in Korea has resulted in the evolution of resistant weeds against SU mixtures (Lee et al., 2012) (Table 2).
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Table 2. Occurrence area of sulfonylurea herbicide resistant weeds in paddy fields. Adapted from Lee et al.(2012). 
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Furthermore, the resistance of barnyard grass to ACCase and ALS inhibitors was confirmed in 2008. The repeated use of ACCase and ALS inhibitors for barnyard grass control in rice led to the evolution of herbicide-resistant barnyard grass. Moreover, SU herbicides like pyrazosulfuron-ethyl and imazosulfuron, which are effective against barnyardgrass, can be associated with the resistance of Echinochloa oryzoides (Park et al., 2015). As a result, ALS and ACCase resistant E. oryzoides have occurred nationwide. (Lee et al., 2017c)
Conyza canadensis is the most frequently developed resistance to glyphosate in many agricultural crops in Korea. In 2017, glyphosate resistance of horseweed to EPSPS synthase inhibitors was discovered in the tangerine orchards of the Jeju province. Six glyphosate resistant horseweeds out of 18 biotypes were found at the recommended rate of 3.28 kg ha-1 (Bo et al., 2016).
At the beginning of 1998, the number of reported herbicide-resistant weed species began to increase rapidly in Korea. Today, herbicide-resistant weeds have been reported in 15 weed species (Table 3). Despite the rapid expansion of herbicide resistance, there is no organization like WAHRI (Western Australian Herbicide Resistance Initiative) or HRAC (Herbicide Resistance Action Committee in the U.S.A) so far in Korea, and furthermore, research in this area has been decreasing rapidly.
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Table 3. Reported herbicide resistant weeds of Korea (Source: Heap, 2017). 
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ALS, acetolactate synthase; ACC, Acetyl-CoA carboxylase; EPSPS, 5-enolpyruvyl-shikimate synthase. |
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Therefore, theoretical education and training of farmers are very important to control resistant weeds. The selection and application of herbicides with alternative modes of action would be much more effective to manage resistant weeds.
Factors inducing herbicide resistance in selection-biotype
Many weeds contain the modified genetic variation that enables them to survive under various environmental conditions. Most herbicides affect a specific site of action, the weed emergence period, or the seed bank duration; thus, there is potential for the utilization of alternative control measures (Greesel, 1978). Generally, weed species that lead to less resistance development have a slower generation time, an incomplete selection pressure for most herbicides, an ability to adapt to a changing environment, a lower fitness for their resistant biotypes, and an extended seed dormancy in the soil. These factors increase the number of susceptible biotypes in the population.
The following factors can stimulate the development of herbicide resistance in selection-biotypes.
Selection pressure by herbicides
In a species, the evolution of a resistant population appears in response to selection pressure imposed by herbicides sharing the same site of action. It is the selection pressure imposed by the herbicide that determines the enrichment of a weed population with resistant individuals.
Persistence of herbicides in the soil
Curran (2001) stated that soil persistence or soil residual life is the length of time of an active herbicide remains in the soil. Herbicides with a long residual effect exert selection pressure on weed populations longer than the herbicides that easily dissipate in the soil. Herbicides change their potential to persist in the soil. If the herbicide is not very persistent, the seed bank present in the soil may decrease the probability of proliferation of the resistant biotypes by keeping an elevated population of susceptible individuals that germinate and reproduce once the herbicide has lost its biological effect. Some herbicide families that are persistent in the soil include triazines, sulfonylureas, isoxazolidiones, imidazolinones, and pyridine which are plant growth regulators.
Soil factors
Soil factors that induce herbicide resistance in selection-biotypes include soil composition (texture), soil chemistry (pH), and microbial activity. Soil composition affects the herbicidal activity and persistence through soil-herbicide binding (adsorption), leaching, and vapour loss (volatilization). Naturally, high clay soils and organic matter have a greater potential to bind the herbicide to soil particles, with the result of a decrease in the leaching and loss of volatilization (De Prado et al., 1997).
Soil pH can influence the persistence of some herbicides, especially the triazines and sulfonylureas. In higher-pH soils (above 7.0), lesser amounts of these herbicides are bound to soil particles making them more available for plant uptake. Thus, in higher-pH soils, triazine and sulfonylurea herbicides persist longer, and a greater amount is available for plant uptake. Low pH also can affect the persistence of both the triazine and sulfonylurea herbicides. In acid soils, herbicides like atrazine become bound to soil particles, making them unavailable for weed control, but at the same time, they are chemically degraded more quickly.
Degradation processes by soil microorganisms are the most important pathways responsible for the breakdown of herbicides. The types of microorganisms (fungi, bacteria, protozoans, etc.) and their relative numbers determine how quickly decomposition occurs.
Climatic factors
Climatic variables influencing herbicide resistance in selection-biotypes include moisture, temperature, and sunlight. Herbicide degradation rates generally increase when the temperature and soil moisture increase. Sunlight is also an important factor in herbicide degradation. Photodecomposition or degradation catalyzed by sunlight (photolysis) occurs especially in a liquid solution (i.e., water) or on plant leaf surfaces. Sensitivity to sunlight and losses through volatilization are the primary reasons for incorporating dinitroanilines at the application time of herbicides.
Biological factors
Although the herbicide resistance problem has become worse in recent years, the new herbicide resistance genes are found at a very low frequency within the population. Therefore, it is logical to conclude that if the resistant individuals were more fit in the absence of selective pressure (herbicide), they would be the dominant type within the population, and the herbicide would never have effectively controlled the weed species in the first place. Therefore, fitness could be described as reproductive success or the gene proportion left from the genetic pool of a population. Its two main components are survival and reproduction (Holt, 1992).
Herbicide properties
The chemical properties of herbicides include water solubility, vapour pressure, and the susceptibility of the molecule to chemical or microbial alteration or degradation.
When an herbicide is dissolved in water, leaching is induced and moves down through the soil profile. A leaching herbicide may readily be carried away from the crop and weed germination zones.
The vapour pressure of an herbicide determines its volatility. Volatilization is the process, whereby an herbicide changes to a gas from a liquid or solid. Volatile herbicides with higher vapour pressures dissipate more rapidly than herbicides with lower vapour pressures.
The chemical structure of an herbicide dictates how the herbicide will degrade in the soil. Some herbicides are rapidly decomposed by microorganisms if the right kind and number are present and the soil conditions are favourable for their growth. However, some herbicides are prone to chemical reactions. For example, members of the sulfonylurea herbicides are degraded through chemical hydrolysis and microbial processes.
Herbicide resistance management
Early detection of resistance makes management easier. Unfortunately, the features of resistant and susceptible plants are similar, and resistance is often not detected until the resistant biotype has spread to 30% of the field. Therefore, using proactive approaches toward diverse weed control tactics is the most effective way to manage herbicide-resistant biotypes (Powles and Yu, 2010).
Cultivation practices associated with high selection pressure like the following must be avoided: use of very persistent herbicides, use of elevated concentrations, regular applications of only one herbicide and finally, mono-cultures that depend solely on chemical methods for the elimination of weeds.
Selection and use of herbicides
Herbicides with different mechanisms of action should be rotated. More than two consecutive uses of herbicides which have the same site of action should be avoided in the same place (Powles and Shaner, 2001). Two consecutive uses of an herbicide mean a single herbicide application for two years or two split applications during one year. The herbicides and alternative methods used must be active against the target weed.
Minimize the use of long-soil residual life herbicides. Susceptible plants emerging later in the season following the use of a long-residual herbicide are exposed to the herbicide, thereby increasing selection pressure. To manage glyphosate-resistant weeds in cropping systems, it is recommended to use a combination of short-term residual herbicides with post-emergence herbicides.
Apply herbicides evenly and accurately, and use of the labeled application rates is recommended. The conditions of metabolic resistance can increase when the application rates are lower than the labeled rates. Using rates that are higher than the labeled rates is illegal and can also enhance selection pressure for resistance. Herbicide preparation in tank-mixed, prepackaged or sequential mixtures can cause multiple sites of action which are recommended. Both herbicides must have a substantial activity against potentially resistant weeds to be effective.
Conclusion
Herbicide resistance in weeds is related to many factors. However, herbicides are chemical resources of great utility aiding in crop production, and they should be used wisely to minimize the spread of resistance. To delay, avoid, or combat widespread herbicide resistance, it is recommended to use herbicides with restraint within IWM (Integrated Weed Management) strategies which minimize the selection pressures for herbicide resistance. Biological and evolutionary realities dictate that this is the only sensible way forward.
Acknowledgements
This work was carried out with the support of the “Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ01245703)” Rural Development Administration, Republic of Korea
Authors Information
Kee Woong Park, https://orcid.org/0000-0003-0053-9543
Aung Bo Bo, https://orcid.org/0000-0001-7579-3429
Ok Jae Won, Chungnam National Univeristy, Doctor of Philosophy
WeiQiang Jia, Chungnam National Univeristy, Ph.D. student
Hye Jin Yun, Chungnam National Univeristy, Researcher
Botir Khaitov, Chungnam National Univeristy, Senior researcher
Thi Hien Le, Chungnam National Univeristy, Ph.D. student
Mirjalol Umurzokov, Chungnam National Univeristy, Master student
Farrukh Ruziev, Chungnam National Univeristy, Master student
Min Ju Lim, Chungnam National Univeristy, Researcher
Kwang Min Cho, https://orcid.org/0000-0003-0537-2164
In Ho Jeong, Chungnam National Univeristy, Ph.D. student
Jeung Joo Lee, Gyeongsang National University, Professor
