**15. Introduction of the group of carboxamides and triple formulations for the control of soybean rust**

In 2012–2013, new fungicides belonging to the Carboxamide group were introduced, which have a specific mode of action, inhibiting fungal respiration, of complex II - succinate dehydrogenase (SDHI), to control ASR [153]. In Brazil, the three fungicides of the carboxamide group available on the market are bixafen, fluxopyiraxade and benzovindiflupyr. Fungicides benzovindiflupyr, bixafen, fluxapyroxad, furametpyr, isopyrazam, penflufen, penthiopyrad and silkxane, resent a medium to high risk for resistance. Numerous cases of resistance to other pathogens have already been documented for the carboxamide group in other countries [147–150, 153]. It is concluded that the introduction of this fungicide group, for the control of ASR, probably will not solve the problem, since they present a specific mode of action, subject to resistance in the population of *Phakopsora pachyrhizi.* Due to these facts, the fungicides of this group, were not recommended for use alone, in the control of rust. Hence the associations or triple mixtures, for use in soybean crops and for the target *Phakopsora pachyrhizi*, arose. In the years 2013/14, there was the registration of triple mixtures, involving fungicides from the groups DMI's + QoI's + SDHI's. The fungicides of the SDHI group, launched on the market, to compose the triple mixtures with triazoles and strobilurins were: benzovindiflupir and fluxpyroxade, bixafen [33, 36, 147–150].

### **16. Emergence of proticonazole from the DMI***'***s group**

In the period comprising 2013–2015, a new fungicide from the DMI's group, protioconazole, appeared. From the beginning of monitoring until its launch on the market, protioconazole has shown the lowest effective concentration values 50 (EC50) in the rust monitoring program. The introduction of this fungicide on the market was the result of hundreds of experiments, conducted in demonstration's areas, from different soy producing regions in Brazil. The protioconazole was then evaluated in a mixture with the QoI fungicide, trifloxystrobin. The comparison was made with fungicides launched on the market, such as the combinations of strobilurins (QoI) and carboxamides (SDHI). Because it is a fungicide, composed of an innovative active ingredient with differentiated binding at the fungus action site, protioconazole constituted the new generation, in the chemical group of DMI's, being chemically classified as triazolintione (Frac classification on mode of action 2014 - www.frac.info). The first studies in Brazil with protioconazole to control soybean rust were carried out by Furtado et al. [103]. The combination protioconazole + trifloxystrobin acts in two ways: 1. in the control of Asian soybean rust, and 2. in the disease complex (such as target spot, powdery mildew, molasses, anthracnose, and end-of-cycle diseases). Therefore, its use is recommended preventively, in the first application or in the first two, when the plan of use of foliar fungicides, is of more than two applications. In this way, it is possible to explore the spectrum of action of this fungicide well, starting in a robust way the prevention

and control of soybean rust and, consequently, an improvement in the performance of the subsequent fungicide.

### **17. Introduction of the dithiocarbamate group to control Asian soybean rust**

In the years 2014 to 2015, the idea of introducing multi-site fungicides into the ASR control programs began to be considered, such as mancozeb, chlorothalonil and others. The introduction of multisite fungicides in ASR control programs could be an especially important tool for the management of resistance to *Phakopsora pachyrhizi*, with the potential to preserve the useful life of specific fungicides DMI's, Qo'sI and SDHI ', s in soybean culture [144, 153]. Multisite fungicides (mancozeb, chlorothalonil, metiram and others) have the great advantage, because in addition to being of low price, they act in multiple sites of action in the fungal cell, interfering with numerous metabolic processes of the fungus, and consequently, resistance to fungicide group would be rare or non-existent [97]. Recent work involving mancozeb, in the control of ASR was developed in Uberlândia - MG and in Rio Verde - Goiás, demonstrated that the product has the potential to control the disease, even in isolated applications [101, 116] (**Figure 4**). Multisite fungicides, such as mancozeb, therefore have the chance to be strong allies in the defense against Asian soybean rust.

Studies carried out at the Federal University of Viçosa on the control of ASR, with fungicides from the triazole group (DMI) + strobilurins (QoI) associated with multisite fungicides (MSF) mancozeb, chlorothalonil or met, in the agricultural years 2013 to 2015, performed by Ponce et al. [90], showed that the association of DMI and QoI with MSF (Alves and [99]), in different environmental conditions,

#### **Figure 4.**

*Residual effects of DMI and QoI, alone or in mixture and multi-site fungicides on ASR in the greenhouse. Source: Ponce et al. [90]. 1. Control; 2. Epoxiconazole + Pyraclostrobin (33.0 + 10.2 g a.i./ha); 3. Cyproconazole + Trifloxystrobin (16.8.0 + 7.2 g a.i./ha); 4. Protioconazole + Trifloxystrobin (28.0 + 16.0 g a. i./ha); 5. Cyproconazole + Azoxystrobin (18.0 + 7.2.0 g a.i./ha) + Nimbus (0.5% v/v); 6. Pyraclostrobin (75.0 g a.i./ha); 7. Mancozeb (240 g a.i./ha); 8. Chlorothalonil (150 g a.i./ha); 9. Metiram + Piraclostrobin (400 g a.i./ha), 10. Tebuconazol + Trifloxistrobina (100.0 + 50.0 g a.i./ha). The bars represent the standard errors of the means. Two experiments were conducted with consistent results; results from one representative experiment are shown. AUDPC – Area under disease progress curve; \*leaf fall – (%). Source: Ponce et al. [90].*

*Etiology, Epidemiology and Management of Asian Soybean Rust (ASR) in Brazil… DOI: http://dx.doi.org/10.5772/intechopen.97686*

#### **Figure 5.**

*Effect of doses Epoxiconazole with Pyraclostrobin mixtured with multi-site fungicides, on soybean grain yield. Source: Ponce et al. [90]. 1. Control; 2. Epoxiconazole + Pyraclostrobin (33.2 + 10.2 g a.i./ha) associated with Mancozeb (1400 g a.i./ha); 3. Epoxiconazole + Pyraclostrobin (33.2 + 10.2 g a.i./ha) associated with Chlorothalonil (1500 g a.i./ha); 4. Epoxiconazole + Pyraclostrobin (33.2 + 10.2 g a.i./ha) associated with Metiram + Pyraclostrobin (1100 + 100 g a.i./ha); 5. Epoxiconazole + Pyraclostrobin (49.8 + 15.3 g a.i./ha) associated with Mancozeb (1400 g a.i./ha, 3.0 kg c.p./ha); 6. Epoxiconazole + Pyraclostrobin (opera SC; 33.2 + 10.2 g a.i./ha, 0.5 L c.p./ha) associated with Chlorothalonil (1500 g a.i./ha); 7. Epoxiconazole + Pyraclostrobin (33.2 + 10.2 g a.i./ha) associated with Metiram + Pyraclostrobin (1100 + 100 g. a.i./ha); 8. Epoxiconazole + Pyraclostrobin (66.5 + 20.5 g a.i./ha) associated with Mancozeb (1400 g. a.i./ha); 9. Epoxiconazole + Pyraclostrobin (133.0 + 41.0 g a.i./ha) associated with Chlorothalonil (1500 g. a.i./ha); 10. Epoxiconazole + Pyraclostrobin (66.5 + 20.5 g a.i./ha) associated with Metiram + Pyraclostrobin (1100 + 100 g a.i./ha). CV = 18.3%. The bars represent the standard errors of the means. Two experiments were conducted with consistent results; results from one representative experiment are shown. \*yield gain – Was obtained in relation to the control treatment. Source: Ponce et al. [90].*

improved the efficacy in the control of the disease and the productivity of the soybean (**Figure 5**). In the greenhouse, triazole fungicides mixed with strobilurin associated with MSF effectively controlled FAS, applied before inoculation (protective effect). On the other hand, triazoles or strobilurins were not effective in controlling ASR in some cultivation areas in Brazil [116]). In this situation, the use of multisites such as mancozeb was providential [33, 116]. There are two possible explanations for this hiring: 1st. failures in the application of fungicides in the field. The application technology is based on three premises: time of application, environmental conditions, and the target to be reached. These are the points that are generally overlooked by producers when applying fungicides, 2nd. the fungus may have acquired resistance to triazole or strobilurin in the field, where soybeans were grown extensively, in the savana's region, when such fungicides were applied alone. The anastomosis of germ tubes, and the migration of nuclei from the hyphae of germ tubes of the soybean rust pathogen, *Phakopsora pachyrhizi*, may explain, how the fungus recombines its genetic material, and develops resistance to fungicides with specific mode of action [154]. It is possible that this mechanism could occur in nature, due to the fact that millions and millions of urediniospores are produced in soybean leaves, in the field and are then dispersed by the wind.

Based on the results obtained, three field experiments were carried out (doses of triazoles with strobilurins associated with MSF (mancozeb, chlorothalonil and metiram) [90]. The hypothesis is that the fungicides of the DMI's and QoI's groups may mixed with MSF's to improve ASR control and increase soybean productivity.

The results showed that the average ASR control with the application of triazolewith strobilurin associated with protective fungicides (mancozeb, chlorothalonil and metiram) was 70.2%. The efficiency of rust control was not higher, because the 04 products were applied after the beginning of the disease epidemic in the field. The 05 field tests were sprayed, when the disease severity had already reached 2.0 to 5.0%, 06 on the leaves of the lower part of the plants. This result shows that any of the three 07 protective fungicides can be used in the mixture with epoxiconazole with piraclostrobin or cyproconazole with azoxystrobin [90]. In general, the DMI's + QoI's fungicides associated with MSF had an efficiency greater than 68.0% of control and produced more than 70.0% of the control (control). These results show that it is possible to control ASR even after the disease severity has reached 2.0 to 5.0%, at the time of plant spraying. In this work, the protective fungicides mancozeb and chlorothalonil associated with epoxiconazole + pyraclostrobin (0.5 kg bw/ha) or cyproconazole + azoxystrobin (0.30 kg bw/ha) increased the yield of soybeans by 89.5% and 109, 0%, respectively. Based on the information above, it is suggested that the application of triazole and strobirulin associated with FMS, starting at the stages of soybean culture (V9 or R1, R2), may promote better control of the disease, especially in the leaves at the bottom of the plant, which is the main source of inoculum, for the upper part and for the whole field. Therefore, the combination of fungicides from the DMI + QoI or SDHI group, associated with MSF, can be recommended as a new strategy for the control of ASR in the short and long term. In addition, due to the residual effect of multisite fungicides [10, 33, 98] on soybean leaves, (mancozeb, chlorothalonil and metiram) can promote greater longevity of the DMI, QoI and SDHI molecules and decrease the number of applications.

The addition of mancozeb to reinforce the fight against fungal resistance is not a new strategy. Mancozeb has been included in mixtures, to contribute to the management of resistance, and to expand the spectrum of fungicides with specific mode of action, for numerous plant diseases. To stabilize ASR control, the same strategy could be used for soybeans, to chemically manage ASR. Examples of fungicides that are already used in mixture with mancozeb include benalaxyl, cymoxanil, dimetomorph, famoxadone, fenamidone, folpet, fosetil-aluminum, iprovalicarb, mandipropamide, metalaxyl and zoxamide. Likewise, this could be followed in the control of ASR, both in Brazil and elsewhere. To reinforce the role of mancozeb, in anti-resistance strategies, in the control of fungal diseases, in more than six decades of continuous use, they have been recorded in more than 70 cultures and in 400different diseases [144, 153]. The introduction of MSF in the ASR control program can be an important tool for managing resistance. Such fungicides have the potential to preserve the useful life of specific fungicides, such as (DMI, QoI and SDHI), in soybean crops.

It was observed that the fungicides of the DMI's group (tebuconazole, epoxiconazole) and the QoI's (azoxystrobin) alone, lost about 40 to 50% of efficiency, in the control of ASR, during this period. The percentage of control of mixtures of DMI's with QoI's ranged from 75% (highest level of control) to 55% (lowest level of control). For the fungicides tebuconazole, cyproconazole and azoxystrobin applied alone, the highest level of control in 2010/2011 was 56% and the lowest 19%. The introduction of fungicides of the SDHI group (bixafen, benzovindiflupir and fluxapiroxad) associated with DMI (protioconazole) and Qo's (picoxystrobin, trifloxystrobin) in triple mixes and in double mixtures

*Etiology, Epidemiology and Management of Asian Soybean Rust (ASR) in Brazil… DOI: http://dx.doi.org/10.5772/intechopen.97686*

(trifloxystrobin + fluxapiroxad + benzoxystrin + maxoxystrobin of control ranging from 69 to 82% (**Table 2**). The most efficient combinations in the control of ASR were those that 08 had the fungicides of the SDHI group in double mixture, with fungicides of the QoI 09 group (pyraclostrobin and azoxystrobin). Therefore, these results suggest that the addition of fungicides from the SDHI group were more efficient both in the control and in the productivity of soybeans (**Table 3**). The highest yields corresponded to the groups' fungicides, which provided the best controls for ASR. Therefore, there was a correlation between ASR control and productivity. The highest yields also corresponded to the mixtures, which had the participation of the fungicides of the SDHI group (bixafen, benzovindiflupyr and fluxapiroxad). In disease control programs, they are often applied as 'dressings' (**Table 2**). **Table 2** shows us that rust control must be done preventively.


*Source: Godoy et al. [113]*.

*Difference between the production of the check and the best treatments were: Application without symptoms) - 52% and with symptoms - 34%*.

#### **Table 2.**

*Reduction of soybean productivity, in different regions with application of fungicides, before the first symptoms and after the Asian soybean rust (ASR) entry in the crop in many states of Brazil.*


#### **Table 3.**

*Percent of control (%) and Yield for double mixtures and casings used to control Asian soybean rust, in 2015/2016.*

**Table 2** summarizes the results of three agricultural years of studies, with fungicides DMI's, QoL's, SDHI's and dithiocarbamate in various regions of the country carried out in 2010/2011 until 2015/2016 [36, 113, 114, 155].
