**3. History and status of herbicide resistance**

The rapid acceptance of GR crops, but not only, the addition of new productive areas and the increasing difficulty in obtaining labor in the fields, has established herbicides as the main control tool, even in integrated systems of weed management. This almost exclusive dependence on herbicides for weed management has contributed to the selection of herbicide resistant weeds with higher frequency. Herbicide resistance is the inherited ability of a plant to survive following application of the commercially used dose of the herbicide recommended for its control [24]. Currently 262 weeds (152 dicots and 110 monocots) have presented 512 unique cases (species x site of action) of herbicide resistance worldwide in 93 crops in 70 countries [11]. In Brazil, there are 51 weed species resistant to herbicides confirmed.

The Brazilian situation of weed resistant to herbicides, mainly to the acetoacetate synthase (ALS) and acetyl coenzyme A carboxylase (ACCase) inhibitors, in conventional soybean cultivation in the mid-2000s was already considered unsustainable due to control difficulties, high cost and low efficiency of the available herbicides to control weed resistant species. The solution to this problem was the introduction of GR soybean varieties [23, 25]. Therefore, to understand the current status of herbicide resistance, it is important to note that GR crops were officially approved in 2005 in Brazil, although GR soybean was irregularly introduced and cultivated in Rio Grande do Sul since 2000. Therefore, the chronological appearance of herbicide resistant weeds is divided into two periods: the pre-glyphosate era preceding 2005 when the use of herbicides was more diversified, and the post-glyphosate era, beginning after approval of GR crops involving an almost exclusive use of glyphosate. In the pre-glyphosate era, from 1993 to 2004, 16 cases were reported, of which only one case presented multiple resistance to two sites of action. In the post-glyphosate era, 35 cases have been reported, of which 16 are cases of multiple resistance. The weed genera with the most resistance cases are *Amaranthus* (7), *Conyza* (8), and *Lolium* (5) (**Figure 4**).

The main groups of herbicides with resistance are the ALS, ACCase, EPSPs, and PSII inhibitors with 30, 9, 16, and 7 cases, respectively (**Figure 5A**). The crop systems with more frequency of herbicide resistance were soybean (30), maize (12), rice (10), wheat (9), and cotton (8) (**Figure 5B**). The Southern, comprising the states of Paraná, Santa Catarina and Rio Grande do Sul, and the Central-West (only in Mato Grosso and Mato Grosso do Sul) regions present 82% of the cases, being Paraná the state where more cases of herbicide resistance were reported (**Figure 5C**). Most of these cases were found in GR crop fields and occurred after 2005, i.e., in the post-glyphosate era, evidencing the drastic changes that GR crop technology caused in weed management.

#### **Figure 4.**

*History of reports of herbicide-resistant weeds in Brazil. Vertical bar indicates the official introduction of transgenic crops resistant to glyphosate. Chart was constructed from the information available in the International Survey of Herbicide Resistant Weeds database [11].*

#### **3.1 Resistance to ALS inhibitors**

The first cases of resistance to ALS inhibitors were *Euphorbia heterophylla* and *Bidens pilosa* reported in 1993 in soybean areas in the states of Mato Grosso do Sul and Rio Grande do Sul, which showed cross-resistance to sulfonylureas and imidazolinones [26]. After, resistant biotypes of *B. subalternans* (1996) [27], *Parthenium hysterophorus* (2004) [28], *Conyza sumatrensis* (2011) [29] and *Ageratum conyzoides* (2013) were found in Paraná. The latter species was also reported in cotton in Mato Grosso [11]. However, the greatest resistance challenges to ALS inhibitors are found in irrigated rice cultivation. The species reported with ALS resistance in this culture are: *Sagittaria montevidensis* (1999) [30], *Echinochloa* sp. (1999) [31], *Cyperus difformis* (2000) [32], *Fimbristylis miliaceae* (2001), *Oryza sativa* (2006), and *Cyperus iria* (2014) [33] in Rio Grande do Sul and Santa Catarina.

Cases of resistance in rice cultivation are associated with the rapid adoption of Clearfield® technology (crops tolerant to imidazolinones, a chemical group of ALS inhibitors), which were introduced in 2002 in areas of southern Brazil [34]. Although the emergence of new resistant species after the adoption of Clearfield® cultivars did not increase significantly, the dispersion of weed populations resistant to ALS inhibitors, mainly of red rice, was favored by genetic flow of cultivated rice to red rice, representing a great agricultural, economic, and social restriction in the use of Clearfield® technology [35].

Other specific, but not least, cases of resistance to ALS inhibitors are *Raphanus sativus* (2001), *Lolium multiflorum* (2010), and *R. raphanistrum* (2013), found in wheat and barley in Rio Grande do Sul and Paraná; and *Amaranthus retroflexus* (2012) in cotton in the states of Mato Grosso, Mato Grosso do Sul and Goiás [11, 36, 37].

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*DOI: http://dx.doi.org/10.5772/intechopen.91236*

**3.2 Resistance to EPSPs inhibitors**

**Figure 5.**

*Weeds database [11].*

Currently, nine weed species have been reported with glyphosate resistance in Brazil, some of these species have multiple resistance to other modes of action [11]. *Lolium multiflorum* (2003) was the first species identified with glyphosate resistance in orchards and vineyards from Rio Grande do Sul [38]. After, *Conyza bonariensis* (2005), *C. canadensis* (2005) [39], *C. sumatrensis* (2010) [40], *Digitaria insularis* (2008) [12], *Chloris elata* (2014) [13], *Amaranthus palmeri* (2015) [14], *Eleusine indica* [15], and *A. hybridus* (2018) [11] were identified with this resistance mainly in maize and soybean, and wheat fields, but also in citrus and coffee orchards in the states of Mato Grosso, Paraná, Rio Grande do Sul and São Paulo. With the exception of *L. multiflorum*, the selection of glyphosate resistance in these species is related to the use of GR cultivars, which has also influenced their dispersion throughout the country. Resistant populations of *L. multiflorm* have gone from infesting apple orchards and vineyards to invading GR-soybean fields in the southern states of Brazil [41]. The species of the genus *Conyza*, which have a high invasive potential due to the large seed production, the rapid and high germination capacity, cause great damage to agriculture, and due to their poor interspecific differentiation, it can be an exchange of resistant alleles between species [42]. However, *D. insularis* has been, among glyphosate resistant species, one of the main problems to be faced; therefore, greater efforts have been made to characterize the factors involved in its resistance, dispersal and management [12, 43–48]. Molecular studies showed that the first glyphosate resistant *D. insularis* populations found in the country (Guairá**—**Paraná) came from Paraguay

*History of reports of herbicide-resistant weeds in Brazil per mode of action of herbicide (A), crop situation (B), and state of first record (C). MT/MS are the abbreviation of the states Mato Grosso and Mato Grosso do Sul. Charts were constructed from the information available in the International Survey of Herbicide Resistant*  *Herbicide Resistance in Brazil: Status, Impacts, and Future Challenges DOI: http://dx.doi.org/10.5772/intechopen.91236*

**Figure 5.**

*Pests, Weeds and Diseases in Agricultural Crop and Animal Husbandry Production*

The first cases of resistance to ALS inhibitors were *Euphorbia heterophylla* and *Bidens pilosa* reported in 1993 in soybean areas in the states of Mato Grosso do Sul and Rio Grande do Sul, which showed cross-resistance to sulfonylureas and imidazolinones [26]. After, resistant biotypes of *B. subalternans* (1996) [27], *Parthenium hysterophorus* (2004) [28], *Conyza sumatrensis* (2011) [29] and *Ageratum conyzoides* (2013) were found in Paraná. The latter species was also reported in cotton in Mato Grosso [11]. However, the greatest resistance challenges to ALS inhibitors are found in irrigated rice cultivation. The species reported with ALS resistance in this culture are: *Sagittaria montevidensis* (1999) [30], *Echinochloa* sp. (1999) [31], *Cyperus difformis* (2000) [32], *Fimbristylis miliaceae* (2001), *Oryza sativa* (2006), and *Cyperus iria*

*History of reports of herbicide-resistant weeds in Brazil. Vertical bar indicates the official introduction of transgenic crops resistant to glyphosate. Chart was constructed from the information available in the* 

Cases of resistance in rice cultivation are associated with the rapid adoption of Clearfield® technology (crops tolerant to imidazolinones, a chemical group of ALS inhibitors), which were introduced in 2002 in areas of southern Brazil [34]. Although the emergence of new resistant species after the adoption of Clearfield® cultivars did not increase significantly, the dispersion of weed populations resistant to ALS inhibitors, mainly of red rice, was favored by genetic flow of cultivated rice to red rice, representing a great agricultural, economic, and social restriction in the

Other specific, but not least, cases of resistance to ALS inhibitors are *Raphanus sativus* (2001), *Lolium multiflorum* (2010), and *R. raphanistrum* (2013), found in wheat and barley in Rio Grande do Sul and Paraná; and *Amaranthus retroflexus* (2012) in cotton in the states of Mato Grosso, Mato Grosso do Sul and

**158**

Goiás [11, 36, 37].

**3.1 Resistance to ALS inhibitors**

*International Survey of Herbicide Resistant Weeds database [11].*

**Figure 4.**

use of Clearfield® technology [35].

(2014) [33] in Rio Grande do Sul and Santa Catarina.

*History of reports of herbicide-resistant weeds in Brazil per mode of action of herbicide (A), crop situation (B), and state of first record (C). MT/MS are the abbreviation of the states Mato Grosso and Mato Grosso do Sul. Charts were constructed from the information available in the International Survey of Herbicide Resistant Weeds database [11].*

#### **3.2 Resistance to EPSPs inhibitors**

Currently, nine weed species have been reported with glyphosate resistance in Brazil, some of these species have multiple resistance to other modes of action [11]. *Lolium multiflorum* (2003) was the first species identified with glyphosate resistance in orchards and vineyards from Rio Grande do Sul [38]. After, *Conyza bonariensis* (2005), *C. canadensis* (2005) [39], *C. sumatrensis* (2010) [40], *Digitaria insularis* (2008) [12], *Chloris elata* (2014) [13], *Amaranthus palmeri* (2015) [14], *Eleusine indica* [15], and *A. hybridus* (2018) [11] were identified with this resistance mainly in maize and soybean, and wheat fields, but also in citrus and coffee orchards in the states of Mato Grosso, Paraná, Rio Grande do Sul and São Paulo.

With the exception of *L. multiflorum*, the selection of glyphosate resistance in these species is related to the use of GR cultivars, which has also influenced their dispersion throughout the country. Resistant populations of *L. multiflorm* have gone from infesting apple orchards and vineyards to invading GR-soybean fields in the southern states of Brazil [41]. The species of the genus *Conyza*, which have a high invasive potential due to the large seed production, the rapid and high germination capacity, cause great damage to agriculture, and due to their poor interspecific differentiation, it can be an exchange of resistant alleles between species [42]. However, *D. insularis* has been, among glyphosate resistant species, one of the main problems to be faced; therefore, greater efforts have been made to characterize the factors involved in its resistance, dispersal and management [12, 43–48]. Molecular studies showed that the first glyphosate resistant *D. insularis* populations found in the country (Guairá**—**Paraná) came from Paraguay

and were dispersed to other states of Brazil, partly due to their biology and perennial capacity, but mainly due to anthropogenic activities, such as the lack of cleanliness of agricultural implements, but also events of independent selection [47, 48].

Other weeds that pose a major challenge to Brazilian agriculture are species of the genus *Amaranthus*, as they are often reported with glyphosate resistance in GR fields in the United States and Argentina [49]. In addition, *Amaranthus* sp. can hybridize interspecifically facilitating dispersion of resistance alleles [50]. In Brazil, *A. palmeri* was reported to have glyphosate resistance in 2015 [11], when its multiple resistance to the ALS inhibitors was also corroborated [14]. However, the Instituto Mato-Grossense do Algodão had records of the occurrence of glyphosate resistant populations of this species since 2012 in the municipalities of Ipiranga do Norte and Tepurah, Mato Grosso, that was imported from Argentina in cotton harvesting machines in 2011 [51]. Recently, multiple resistance of *A. hybridus* to glyphosate and ALS inhibitors was also confirmed in Rio Grande do Sul in soybeans [11, 52]. With respect to the latter case, there is great concern because it is feared that it has also been introduced from Argentina, where populations of *A. hybridus* with this resistance profile carry mutations in the genes encoding the target enzymes [53]. In the case of glyphosate resistance, it is a triple mutation that confers high levels of resistance and that had not previously been observed in any other species [10, 54]. In addition, in Argentina there are also populations of the species with multiple resistance to 2,4-D and dicamba [55]. Therefore, if it is confirmed that the resistant populations of *A. hybridus* found in Brazil were introduced from Argentina, the scenario faced by Brazilian farmers in the coming years in relation to weed management will be very difficult.

## **3.3 Resistance to ACCase inhibitors**

*Urochloa plantaginea* (1997) [56], *Digitaria ciliaris* (2002) [57], *Eleusine indica* (2003) [58], *Avena fatua* (2010) [11], and *D. insularis* [16] were reported with resistance to ACCase inhibitors, mainly in non-transgenic soybean fields. These findings demonstrate the importance of these herbicides for the control of grasses in soybean fields, due to the low availability of selective herbicides that effectively control these weeds in pre-emergence conditions, allied to the difficulties of using graminicides, since these products have high retention in the organic matter [29].

## **3.4 Resistance to other mechanisms of action**

The majority of herbicide resistance cases reported in Brazil are included in the three groups of herbicides described above, following the global trend. However, cases of resistance to other modes of action have also been found. In 1999, *Echinochloa crus-pavonis* and *E. crus-galli* were reported with resistance to synthetic auxins, specifically quinclorac, in rice fields of Itajai, Santa Catarina [59]. *Amaranthus retroflexus* (2014) and *C. sumatrensis* (2017) were reported with resistance to PPO inhibitors [11]. The first showed fomesafen resistance and it was found in GR-soybean and -cotton fields of Mato Grosso; and *C. sumatrensis* presented resistance to saflufenacil in soybean fields in the western region of Paraná in the municipalities of Palotina and Assis Chateaubriand [11]. This last species had already been confirmed to be resistance to chlorimuron-ethyl (ALS inhibitor) in 2011 [60] and paraquat (PSI inhibitor) in 2016 [61] within the same region.

### **3.5 Cross- and multiple-resistance**

Cross resistance is expressed when a weed resistant biotype shown resistance against two or more herbicides with the same mode of action, and multiple

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*Herbicide Resistance in Brazil: Status, Impacts, and Future Challenges*

resistance occurs when a weed resistant to a given herbicide manifests resistance to two or more different modes of action. Most cases of resistance to ALS inhibitors have cross resistance, that is, weeds resistant to imidazolinones often have a degree of resistance to sulfunylureas and vice versa [29]. *Eleusine indica* resistant to sethoxydim (cyclohexanediones) showed resistance to the ariloxifenoxipropionatos (FOPs) [58], and quinclorac resistant *E. crus-galli* showed cross resistant to others synthetic auxins [11]. Weeds with cross resistance represent a great challenge for Brazilian agricultural sustainability; however, weeds with multiple resistance are

The occurrence of multiple resistance has increased significantly in recent years, and most of the reported cases occurred in the post-glyphosate era. The first case of multiple resistance was *E. heterophylla*, which was found in fields of maize and soybeans in 2004 and showed resistant to triclopyr and fomesafen (ALS + PPO) [62]. In 2009, *E. crus-galli* was found with resistance to synthetic auxins and ALS inhibitors in rice fields in Rio Grande do Sul [34]. Biotypes of *B. subalternans* (2006) and *B. pilosa* (2016) were found to be resistant to atrazine (PSII inhibitors) and ALS inhibitors in soybean and maize fields from Paraná [63]. Among the cases that involves glyphosate resistance are *C. sumatrensis* (2014), *A. palmeri* (2015) and *A. hybridus* (2018) as dicots, that also shown resistance to the ALS inhibitors and were found in soybean fields [11, 14, 60], and *L. multiflorum* (2010), *D. insularis* (2016), and *E. indica* (2016) as monocots with resistance to the ACCase inhibitors. However, the most worrying case is *Conyza sumatrensis* reported in 2017, which was found as being resistant to EPSPs, PSI, PSII, PPO and synthetic auxins in a

This brief account shows the global scenario of the current situation of herbicide resistance in Brazil; however, it is far from reality, because only the first occurrence of a unique case (species x site of action) is reported, while in countries like the United States and Australia, there are multiple reports for the same unique case of herbicide resistant occurring in different regions. For example, the case of *A. palmeri* resistant to glyphosate have more than 30 reports along of the United States [11]. To have an idea of the real problem in Brazil, we have as an example the study conducted by Lopez-Ovejero et al. [45], who determined the frequency and dispersion patterns of glyphosate resistant *D. insularis* revealing the existence of 1299 (of 2596) populations with different resistance levels to this herbicide distributed only in the areas of soybean production. In the scientific-academic environment it is commonly said that it is more difficult to find a population susceptible to the glyphosate of *C. sumatrensis* or *D. insularis* than a resistant one. In addition, from the botanical point of view, more species of the Amaranthaceae, Asteraceae, Cyperaceae, and Poaceae families have high potential to select for resistant to the inhibitors of ALS, ACCase,

Genetic factors such as genetic variability (mutations localized in a single locus), heredity patterns (dominance of genes enable rapid dispersion), type of pollination (cross-pollination allows for greater genetic recombination and recessive alleles are more easily established in autogenous species), flow gene (transfer resistance characteristics to a susceptible population) and number of resistance genes involved; and bioecological factors such as short life cycle, high seed yield, low dormancy, multiple generations per year, mechanism of propagule dispersion, extreme susceptibility to herbicides, population size, and low biodiversity are key factors in the selection of herbicide resistant weed populations [65]. However, in this section

more challenging by reducing chemical alternatives for their control.

GR-soybean field from Assis Chateaubriand-PR [11].

EPSPs, PPO, and synthetic auxin herbicides in the coming years [64].

**4. Herbicide resistance: the problem and the cause**

*DOI: http://dx.doi.org/10.5772/intechopen.91236*

#### *Herbicide Resistance in Brazil: Status, Impacts, and Future Challenges DOI: http://dx.doi.org/10.5772/intechopen.91236*

*Pests, Weeds and Diseases in Agricultural Crop and Animal Husbandry Production*

agricultural implements, but also events of independent selection [47, 48].

coming years in relation to weed management will be very difficult.

*Urochloa plantaginea* (1997) [56], *Digitaria ciliaris* (2002) [57], *Eleusine indica* (2003) [58], *Avena fatua* (2010) [11], and *D. insularis* [16] were reported with resistance to ACCase inhibitors, mainly in non-transgenic soybean fields. These findings demonstrate the importance of these herbicides for the control of grasses in soybean fields, due to the low availability of selective herbicides that effectively control these weeds in pre-emergence conditions, allied to the difficulties of using graminicides, since these products have high retention in the organic matter [29].

The majority of herbicide resistance cases reported in Brazil are included in the three groups of herbicides described above, following the global trend. However, cases of resistance to other modes of action have also been found. In 1999, *Echinochloa crus-pavonis* and *E. crus-galli* were reported with resistance to synthetic auxins, specifically quinclorac, in rice fields of Itajai, Santa Catarina [59]. *Amaranthus retroflexus* (2014) and *C. sumatrensis* (2017) were reported with resistance to PPO inhibitors [11]. The first showed fomesafen resistance and it was found in GR-soybean and -cotton fields of Mato Grosso; and *C. sumatrensis* presented resistance to saflufenacil in soybean fields in the western region of Paraná in the municipalities of Palotina and Assis Chateaubriand [11]. This last species had already been confirmed to be resistance to chlorimuron-ethyl (ALS inhibitor) in 2011 [60] and paraquat (PSI inhibitor) in 2016 [61] within the same region.

Cross resistance is expressed when a weed resistant biotype shown resistance

against two or more herbicides with the same mode of action, and multiple

**3.3 Resistance to ACCase inhibitors**

**3.4 Resistance to other mechanisms of action**

**3.5 Cross- and multiple-resistance**

and were dispersed to other states of Brazil, partly due to their biology and perennial capacity, but mainly due to anthropogenic activities, such as the lack of cleanliness of

Other weeds that pose a major challenge to Brazilian agriculture are species of the genus *Amaranthus*, as they are often reported with glyphosate resistance in GR fields in the United States and Argentina [49]. In addition, *Amaranthus* sp. can hybridize interspecifically facilitating dispersion of resistance alleles [50]. In Brazil, *A. palmeri* was reported to have glyphosate resistance in 2015 [11], when its multiple resistance to the ALS inhibitors was also corroborated [14]. However, the Instituto Mato-Grossense do Algodão had records of the occurrence of glyphosate resistant populations of this species since 2012 in the municipalities of Ipiranga do Norte and Tepurah, Mato Grosso, that was imported from Argentina in cotton harvesting machines in 2011 [51]. Recently, multiple resistance of *A. hybridus* to glyphosate and ALS inhibitors was also confirmed in Rio Grande do Sul in soybeans [11, 52]. With respect to the latter case, there is great concern because it is feared that it has also been introduced from Argentina, where populations of *A. hybridus* with this resistance profile carry mutations in the genes encoding the target enzymes [53]. In the case of glyphosate resistance, it is a triple mutation that confers high levels of resistance and that had not previously been observed in any other species [10, 54]. In addition, in Argentina there are also populations of the species with multiple resistance to 2,4-D and dicamba [55]. Therefore, if it is confirmed that the resistant populations of *A. hybridus* found in Brazil were introduced from Argentina, the scenario faced by Brazilian farmers in the

**160**

resistance occurs when a weed resistant to a given herbicide manifests resistance to two or more different modes of action. Most cases of resistance to ALS inhibitors have cross resistance, that is, weeds resistant to imidazolinones often have a degree of resistance to sulfunylureas and vice versa [29]. *Eleusine indica* resistant to sethoxydim (cyclohexanediones) showed resistance to the ariloxifenoxipropionatos (FOPs) [58], and quinclorac resistant *E. crus-galli* showed cross resistant to others synthetic auxins [11]. Weeds with cross resistance represent a great challenge for Brazilian agricultural sustainability; however, weeds with multiple resistance are more challenging by reducing chemical alternatives for their control.

The occurrence of multiple resistance has increased significantly in recent years, and most of the reported cases occurred in the post-glyphosate era. The first case of multiple resistance was *E. heterophylla*, which was found in fields of maize and soybeans in 2004 and showed resistant to triclopyr and fomesafen (ALS + PPO) [62]. In 2009, *E. crus-galli* was found with resistance to synthetic auxins and ALS inhibitors in rice fields in Rio Grande do Sul [34]. Biotypes of *B. subalternans* (2006) and *B. pilosa* (2016) were found to be resistant to atrazine (PSII inhibitors) and ALS inhibitors in soybean and maize fields from Paraná [63]. Among the cases that involves glyphosate resistance are *C. sumatrensis* (2014), *A. palmeri* (2015) and *A. hybridus* (2018) as dicots, that also shown resistance to the ALS inhibitors and were found in soybean fields [11, 14, 60], and *L. multiflorum* (2010), *D. insularis* (2016), and *E. indica* (2016) as monocots with resistance to the ACCase inhibitors. However, the most worrying case is *Conyza sumatrensis* reported in 2017, which was found as being resistant to EPSPs, PSI, PSII, PPO and synthetic auxins in a GR-soybean field from Assis Chateaubriand-PR [11].

This brief account shows the global scenario of the current situation of herbicide resistance in Brazil; however, it is far from reality, because only the first occurrence of a unique case (species x site of action) is reported, while in countries like the United States and Australia, there are multiple reports for the same unique case of herbicide resistant occurring in different regions. For example, the case of *A. palmeri* resistant to glyphosate have more than 30 reports along of the United States [11]. To have an idea of the real problem in Brazil, we have as an example the study conducted by Lopez-Ovejero et al. [45], who determined the frequency and dispersion patterns of glyphosate resistant *D. insularis* revealing the existence of 1299 (of 2596) populations with different resistance levels to this herbicide distributed only in the areas of soybean production. In the scientific-academic environment it is commonly said that it is more difficult to find a population susceptible to the glyphosate of *C. sumatrensis* or *D. insularis* than a resistant one. In addition, from the botanical point of view, more species of the Amaranthaceae, Asteraceae, Cyperaceae, and Poaceae families have high potential to select for resistant to the inhibitors of ALS, ACCase, EPSPs, PPO, and synthetic auxin herbicides in the coming years [64].
