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Revista mexicana de ciencias agrícolas

versión impresa ISSN 2007-0934

Rev. Mex. Cienc. Agríc vol.9 no.2 Texcoco feb./mar. 2018 


Response of oat genotypes to infection by Puccinia graminis f. sp. Avenae in the high valleys of Mexico

Santos Gerardo Leyva-Mir1 

Héctor Eduardo Villaseñor-Mir2 

Moisés Camacho-Tapia3 

Graciela Dolores Ávila-Quezada4 

Elizabeth García-León3 

Juan Manuel Tovar-Pedraza1  § 

1Departamento de Parasitología Agrícola-Universidad Autónoma Chapingo. Carretera México-Texcoco km 38.5. Texcoco, Estado de México, México. CP. 56230. Tel. 01(595) 9521500, ext. 6304 (;

2Campo Experimental Valle de México-INIFAP. Carretera Los Reyes-Texcoco km 13.5, Coatlinchán, Texcoco, Estado de México, México. CP. 56230. Tel. 01(595) 9212715, ext. 161. (

3Campus Montecillo-Colegio de Postgraduados. Carretera México-Texcoco km 36.5, Texcoco, Estado de México, México CP. 56230 (;

4Facultad de Zootecnia y Ecología-Universidad Autónoma de Chihuahua. Periférico Francisco R. Almada km 1, Chihuahua. CP. 33820. (


Stem rust of oats, caused by Puccinia graminis f. sp. avenae, has increased its incidence and severity significantly in temporal plots distributed in the high valleys of Mexico. The objective of this study was to determine the response of 28 temperate oats genotypes to Puccinia graminis f. sp. avenae infection under field conditions, during the spring-summer 2013 and 2014 cycles. A completely randomized experimental design was used with four replications, and an arrangement of treatments in divided plots. The large plots were five planting dates and the small plots consisted of the 28 oat genotypes. The response variable was the percentage of stem rust damage in each of the genotypes, from the beginning of the disease to the end of each crop cycle. The variety of oats most resistant to stem rust was Diamond R-31, followed by Nodaway, AB177 and Teporaca. While the most susceptible varieties were Guelatao, Tulancingo and Ópalo. Likewise, planting dates 1 (June 23) and 2 (June 30) presented the lowest percentages of disease severity. Additionally, it was observed that the oat grain yield decreases severely in the presence of stem rust and without being controlled with any fungicide.

Keywords: Avena sativa; Puccinia graminis f. sp. avenae; fungicide; severity


La roya del tallo de la avena, causada por Puccinia graminis f. sp. avenae, ha aumentado su incidencia y severidad significativamente en parcelas de temporal distribuidas en Valles Altos de México. El objetivo de este estudio fue de determinar la respuesta de 28 genotipos de avena de temporal a la infección por Puccinia graminis f. sp. avenae bajo condiciones de campo, durante los ciclos primavera-verano 2013 y 2014. Se utilizó un diseño experimental completamente al azar con cuatro repeticiones, y un arreglo de tratamientos en parcelas divididas. Las parcelas grandes fueron cinco fechas de siembra y las parcelas chicas estuvieron constituidas por los 28 genotipos de avena. La variable respuesta fue el porcentaje de daño de roya del tallo en cada uno de los genotipos, desde que se inició la enfermedad hasta el término de cada ciclo del cultivo. La variedad de avena más resistente a la roya del tallo fue Diamante R-31, seguida por Nodaway, AB177 y Teporaca. Mientras que las variedades más susceptibles fueron Guelatao, Tulancingo y Ópalo. Asimismo, las fechas de siembra 1 (23 de junio) y 2 (30 de junio) presentaron los menores porcentajes de severidad de la enfermedad. Adicionalmente, se observó que el rendimiento de grano de avena disminuye severamente en presencia de la roya del tallo y sin ser controlada con algún fungicida.

Palabras clave: Avena sativa; Puccinia graminis f. sp. avenae; fungicida; severidad


In Mexico, the area planted with oats (Avena sativa L.) has increased, although not enough is produced to supply the demands. The area planted with oats in Mexico in 2014 was 833 221 ha distributed in all the agricultural areas of the country (SIAP, 2015). Due to its adaptation to diverse environmental conditions, oats are considered an alternative crop in the high valleys of Mexico and in the semi-arid north-central region, particularly when the onset of the rainy season is delayed or the temperature is low, as planting Traditional crops, such as maize (Zea mays L.) and beans (Phaseolus vulgaris L.), are put at risk (Villaseñor-Mir et al., 2003).

It is important to indicate that oats are an excellent option for the productive reconversion of low productivity lands with livestock aptitude in the regions in which the growing season is short and which are currently used in the production of traditional crops; however, for this crop to become widely used, it is necessary to have varieties suitable for the production of forage and grain with a set of agronomic and phytopathological attributes that minimize the negative effect of the incidence of stem rust (Puccinia graminis f. sp. avenae) and crown rust (Puccinia coronata var. avenae), as well as the occurrence of early frosts and intermittent drought (Villaseñor-Mir et al., 2003).

Worldwide, Puccinia graminis f. sp. avenae is the most destructive pathogen of oat cultivation, since it has caused severe epidemics in the main producing areas of South Africa (van Niekerk et al., 2001), Australia (Keiper et al., 2006; Hake et al., 2008), Canada (Gold-Steinberg et al., 2005; Michell and Fetch, 2011), Sweden (Berlin et al., 2013) and China (Li et al., 2015). In Mexico, stem rust is the disease that most affects the production of oats, since it can diminish the yield up to 50%, because this pathogen affects from the stage of seedling until the filling of the grain, besides they use highly susceptible varieties (Leyva-Mir et al., 2013).

Likewise, the disease is especially important in spring-summer cycles in central Mexico (Leyva-Mir et al., 2013; García-León et al., 2015), which is why these environments may not be suitable for seed production and autumn-winter production in the Mexican Bajío becomes an option (Bobadilla-Meléndez et al., 2013).

The genetic improvement of oats in Mexico began in 1960 and since then the Valley of Mexico Experimental Field (CEVAMEX) of the National Institute of Forestry, Agriculture and Livestock Research (INIFAP) has been the main station where the release of varieties. To date, it has made more than 30 varieties available to farmers, which have been the basis of national production (Villaseñor-Mir et al., 2009). Likewise, the selection criteria of the genetic improvement program of oats in Mexico, have focused mainly on, the greater production of grain, resistance to stem rust, good response in conditions of temporary limitation (drought) and greater tolerance to lodging (Jiménez-González, 1992; Villaseñor-Mir et al., 2009).

The sowing season defines not only the yield and other agronomic aspects of the crop, but also the expression of some attributes of quality, presence or absence of harmful organisms, for which the one that allows obtaining the best yield and quality must be carefully selected (Forsberg and Reeves, 1995). In addition, the sowing season is associated with the duration of the day, solar radiation and temperature, so it is important to identify the most suitable areas for the growth, development and production of the crop. For this reason, the optimal date should be determined in each locality, which will depend on the climate, the incidence of pests and diseases, as well as other factors (Bobadilla-Meléndez et al., 2013).

The objective of this study was to determine the response of 28 temperate oats genotypes from the high valleys of Mexico to Puccinia graminis f. sp. avenae infection, in five sowing dates during the Spring-Summer 2013 and 2014 cycles.

Materials and methods

Study site

The experiment was carried out during the spring-summer (S-S) cycles of 2013 and 2014, in the Valley of Mexico Experimental Field (CEVAMEX), belonging to the National Institute of Forestry, Agriculture and Livestock Research (INIFAP), located in Chapingo, State of Mexico, Mexico at 19° 29’ north latitude and 99° 53’ west longitude, at a height of 2250 meters above sea level, with an average annual rainfall of 640 mm and 15 °C average annual temperature (García, 1981).

Establishment of the experiment

Twenty-eight varieties of oats belonging to the CEVAMEX collection were evaluated under temporary conditions on five sowing dates and with a spacing of 07 days between each date. The first sowing date was June 23, the second on June 30, the third on July 7, the fourth on July 14 and the fifth was on July 21, of the S-S 2013 and 2014 cycles. The preparation of the land consisted of a fallow and a harrowing step with the purpose that the ground would remain soft and thus obtain a uniform germination. Seeding was done manually, at a density of 60 kg ha-1. The presence of the pathogen was allowed to occur naturally, because the environmental conditions where the experiment was carried out are highly favorable for the development of the disease.

We used a completely randomized experimental design with four replications, and an array of treatments in divided plots. The large plots were the five sowing dates and the small plots were constituted by the 28 varieties. Twenty-eight experimental units were established, consisting of four rows with 5 m long × 0.3 m wide, and four repetitions were made of each.

The evaluations were carried out only in the two central rows of each experimental unit and the response variable was the percentage of damage caused by stem rust in each of the oat varieties from the time the disease was disease present until the end of each cycle of the culture. It is worth mentioning that when analyzing the data for a date, the experimental design was completely random; however, when all the dates were analyzed together, a design was chosen in divided plots (Montgomery, 2003).

The incidence and severity data were recorded in all varieties until the end of each cycle; the evaluations were every 8 days in 5 dates and in all varieties.

Variables evaluated

The disease was presented at the beginning of September 2013 and 2014, as of this date the data collection began. In each variety and in each sowing date, the severity was evaluated visually every 8 days until the commercial maturity of the culture using the modified scale of Peterson et al. (1948), which consists in taking values of disease severity from 01 to 100%.

On the other hand, the performance of each of the varieties on each date was evaluated. At the end of the 2013 and 2014 crop cycles, 10 stems were harvested at ground level for each variety and in each of the five planting dates. Later the samples were threshed to obtain the grain yield using an analytical scale, and in this way the grain yield of each of the varieties was compared on each date. In addition, the weight of 1 000 seeds without fungicidal treatment was compared against the weight of 1 000 seeds of the same varieties, but treated with the fungicide tebuconazole (Folicur®, Bayer) at a concentration of 2 mL of commercial product per L of water, sprinkling in total form to the plant during a date of the crop cycle.

Finally, the flowering days were determined by counting the days elapsed from sowing until the time when 50% of the spikelets of each variety reached flowering. While, the days to commercial maturity were obtained by counting the days elapsed from sowing until the moment when the pedicle of the panicle turned yellow.

Statistical analysis

The data obtained from the percentage of severity of all the samplings, in the different sowing dates and in all the varieties during each crop cycle, were adjusted to a model of progress of the epidemic of exponential type with the Curve Expert 2® program. Likewise, with this model an area under the curve of the progress of the disease (ABCPE) was calculated as an integrative parameter using Scientific Work Place 5®. A T test was carried out to determine if there were differences in the ABCPE values of the different varieties in the 5 sowing dates and in both cycles. With the statistical package SAS (Version 9.1) an analysis of variance (Anova) and mean comparisons were performed using the minimum significant difference test (DMS) (α= 0.05), by date (completely random) and an analysis of variance and comparisons of means between dates (divided plots).

Results and discussion

Variety response to infection

The disease was presented at the beginning of September in both years, time when the first pustules were observed on leaves and stems of the susceptible varieties. On the first date the first symptoms were observed and it was disseminated to the other dates. According to the T test, the ABCPE of the two cycles evaluated did not have significant differences; in such a way that the average obtained from the two cycles was used for the analyzes. The Anova carried out with all the varieties in the five sowing dates showed significant differences (p= 0.05).

When comparing means with DMS, it was observed that the variety with the lowest ABCPE in the five sowing dates was Diamante R-31 (Table 1), which coincided with Jiménez-González (1992), who described this variety as one of the most resistant to stem rust for own genes of resistance to different races. Also, the Nodaway, AB177 and Teporaca varieties were also resistant to the infection caused by P. graminis f. sp. avenae, coinciding with what was indicated by Salmeron-Zamora (2001), in the case of the Teporaca variety.

Table 1 Values of area under the disease progress curve (ABCPE) in 28 oat genotypes in 5 planting dates during the Spring-Summer 2013 and 2014 cycles. 

Variety Date 1 Date 2 Date 3 Date 4 Date 5 Mean (combined)
Guelatao 2390.5 2600.5 2776.7 2758 2450 2595.1 a
Tulancingo 2397.5 2671.7 2473.3 2676.3 2467.5 2537.3 ab
Ópalo 2327.5 2460.5 2444.2 2438.3 2397.5 2413.6 abc
Cuauhtemoc 1976.3 1814.2 2279.7 2310 2390.5 2154 abcd
Texas 1629.8 2117.5 2437.2 2362.5 1820 2073 abcde
Pampas 2100 2000.8 1925 2024.2 2310 2072 abcde
Perla 1855 1853.8 2251.7 1894.7 2135 1998 bcdef
Cevamex 1918 2172.3 1919.2 1890 2047.5 1989.4 bcdefg
Huamantla 1890 1556.3 1953 2191 1888.8 1896 cdefgh
Paramo 1935.5 1505 1761.7 2013.7 1731.3 1789.4 defghi
Chihuahua 1830.5 1369.7 2123.3 1534.2 2088.3 1789 defghi
Gema 1697.5 2173.5 1895.8 1575 1417.5 1752 defghi
Babicora 1260 1258.8 1545.8 1890 2286.7 1648 defghij
Obsidiana 1620.5 1235.5 1685.8 1709.2 1843.3 1619 defghij
Tarahumara 1423.3 1305.5 1806 1627.5 1468.8 1526.2 efghijk
Karma 1277.5 1433.8 1370.8 1790.8 1585.5 1491.7 fghijk
Raramuri 1155 1655.5 1674.2 1715 1120 1464 fghijk
Bachiniva 1165.5 1334.7 1510.8 1295 1884.2 1438 ghijkl
Cusihuiriachi 1298.5 1159.7 1265.8 1388.3 1872.5 1397 hijkl
Putnam61 1225 1451.3 1761.6 1295 1242.5 1395.1 hijkl
Papigochi 1018.5 1387.2 1036 1540 1709.2 1338 ijklm
Turquesa 1114.2 1398.8 1212.2 1155 1289.2 1233.9 ijklm
Juchitepec 990.5 990.5 1281 1556.3 1136.3 1191 jklm
Menonita 1008 1194.7 1012.7 1061.7 1610 1177 jklm
Teporaca 1018.5 808.5 850.5 1193.5 1060.5 986.3 klm
AB177 791 779.3 826 1057 980 886.7 l mn
Nodaway 598.5 780.5 784 955.5 940.3 811.8 mn
Diamante R-31 413 402.5 434 434 423.5 421.4 n

*= Means with the same letter in each column are statistically equal (α= 0.05).

The importance of knowing varieties of oats that can serve as a source of resistance to stem rust is key to breeding programs, in addition to the use of resistant varieties is the most used strategy for the control of this disease (Mariscal-Amaro et al., 2010; Leyva-Mir et al., 2013).

The varieties that were most susceptible and had a higher ABCPE were Guelatao, Tulancingo and Opalo. In the case of the Tulancingo variety, it was deferred with that indicated by Castro-Melendrez and Jiménez-González (1981), who considered it to be moderately resistant to stem rust, however, in this investigation it was one of the most susceptible varieties during the two cycles evaluated. Meanwhile, in the case of the Guelatao and Ópalo varieties, our results coincided with those reported by Jimenez-González (1992), who reported these varieties as highly susceptible to stem rust.

Comparison between planting dates

According to the Anova, in the five sowing dates (p= 0.05), there were highly significant differences. Likewise, the comparison of means with DMS (Table 2) indicated that planting dates 1 and 2 had the lowest values of ABCPE (severity of stem rust), coinciding with Tovar (1974), who assured that there is an effect of different dates of sowing on the yield before the attack of stem rust on varieties of oats.

Table 2 Area under the disease progress curve (ABCPE) for each of the 5 sowing dates of 28 oat genotypes during the Spring-Summer 2013 and 2014 cycles. 

Planting dates ABCPE
Date 5 (July 21) 1657.58 a*
Date 4 (July 14) 1643.08 a
Date 3 (July 7) 1619.13 a
Date 2 (June 30) 1471.38 b
Date 1 (June 23) 1431.63 b

*= Means with the same letter in each column are statistically equal (DMS, 0.05).

When analyzing the interactions between each one of the varieties and in all planting dates, it was observed that, in most varieties of oats, dates 1 and 2 could be considered as the best, since they obtained lower ABCPE. It should be noted that some exceptions were found, such as the Gema and Cevamex varieties, where the best sowing date was date 4, as well as the Pampas variety, in which the best sowing date was 3, while in the Raramuri variety was date 5. This shows that there are varieties that are more susceptible to stem rust on certain dates and for this reason the yields of a variety on different dates will depend on the environmental conditions that the disease has to damage the cultivation and decrease the yield, as mentioned by Leyva-Mir et al. (2004).

The results generated in this study can be considered to make decisions about the optimal time to carry out the sowing and thus obtain a higher yield of these 28 oat genotypes under rainfed conditions in the High Valleys of Mexico. Similarly, Bobadilla-Meléndez et al. (2013) verified that planting dates, varieties and densities have a direct influence on the productivity and physical quality of the seed.

Percentage of damage in the last evaluation

Oat varieties evaluated showed an increase in severity from the first to the fourth planting date. Stem rust caused lower percentage of damage in earlier dates compared to later dates that is to say to earlier dates, the oat varieties can escape the attack of rust (Table 3). The above, agrees with the work of Smith (1992), who found that one of the best methods of control of stem rust in oats is to choose the right time to sow and avoid late varieties.

Table 3 Percentage of disease severity caused by Puccinia graminis f. sp. avenae in each of the 28 oat genotypes in the 5 sowing dates evaluated during the Spring-Summer 2013 and 2014 cycles. 

Variety Severity (%) Average (%)
Date 1 Date 2 Date 3 Date 4 Date 5
Texas 61 77 88 90 77 78.6
Nodaway 25 29 28 40 38 32
AB177 30 28 30 38 40 33.2
Putnam61 65 55 80 67 56 64.6
Perla 70 65 85 83 85 77.6
Ópalo 90 85 90 92 90 89.4
Chihuahua 66 50 78 63 80 67.4
Cuauhtémoc 71 67 83 85 88 78.8
Guelatao 93 83 90 93 95 90.8
Tulancingo 90 87 90 88 90 89
Juchitepec 40 38 45 60 45 45.6
Huamantla 75 56 66 78 68 68.6
Diamante R-31 15 15 16 16 15 15.4
Tarahumara 53 48 55 72 51 55.8
Paramo 75 55 65 74 61 66
Gema 80 70 85 80 65 76
Babicora 55 51 65 75 85 66.2
Cusihuiriachi 45 46 55 68 82 59.2
Papigochi 37 51 40 70 65 52.6
Raramuri 55 58 70 80 50 62.6
Karma 50 51 52 80 63 59.2
Cevamex 78 76 73 85 88 80
Menonita 43 46 40 50 70 49.8
Bachiniva 48 53 58 67 77 60.6
Obsidiana 63 48 68 82 77 67.6
Turquesa 50 54 53 50 65 54.4
Pampas 75 73 77 80 85 78
Teporaca 35 30 33 40 43 36.2

The variation in the percentage of damage between varieties shows that each genotype contains genes that give it resistance against the attack of stem rust. For this case we can point out that the Guelatao, Tulancingo, Ópalo, Cuauhtémoc, Texas, Pampas and Perla varieties were the varieties of oats most susceptible to stem rust. While the less susceptible varieties were Diamante R-31, Nodaway, AB177 and Teporaca.

It is important to point out that the majority of oat varieties cultivated in Mexico are susceptible to stem rust, coinciding with Li et al. (2015), who mentioned that the majority of the varieties produced in China and worldwide are susceptible to the pathogen and that they vary widely in the level of response to the disease.

Fungicide treatment

The comparison of the average weight of the 5 sowing dates without fungicide and the date with fungicide of the 1 000 seeds indicated that the yield of grain in the presence of stem rust in all oat varieties tends to decrease when the disease is present, because the fungus disturbs the normal source-demand relationships of the plant by sucking the assimilated ones that go to the developing seeds (Table 4). Smith (1992) found that when P. graminis f. sp. avenae disturbs the epidermis, the plant may dry up, so that the flow of sap does not reach the spike and as a result prematurely matures forming less seed and less weight of the grain.

Table 4 Average weight of 1 000 seeds of 28 varieties of oats harvested during 5 dates of the spring-summer 2013 and 2014 cycles, with and without fungicide treatment. 

Varieties With fungicide 1 date Without fungicide x̄ of 5 dates (%) of loss
Texas 3.3 2.36 28
Nodaway 4.5 3.9 13
Ab-177 4.6 3.96 14
Putnam 61 4.2 3.12 26
Perla 3.4 2.38 30
Ópalo 3.1 1.5 52
Chihuahua 4 3.36 16
Cuauhtémoc 4 2.74 32
Guelatao 3.5 2.78 21
Tulancingo 3.2 2.56 20
Juchitepec 4 3.5 13
Huamantla 3 2.42 19
Diamante R-31 3.5 3.32 5
Tarahumara 3.2 2.6 19
Paramo 5 3.74 25
Gema 4 2.9 28
Babicora 3.4 3.12 8
Cusihuiriachi 4.1 3.8 7
Papigoche 4.4 3.74 15
Raramuri 4.4 3.2 27
Karma 4.1 3.16 23
Cevamex 4.8 3.18 34
Menonita 3.7 3.04 18
Bachiniva 4.4 3.18 28
Obsidiana 4.1 3.24 21
Turquesa 4.4 3.4 23
Pampas 4.3 3.16 27
Teporaca 4.1 3.52 14

In the case of the Opalo variety, which is highly susceptible to infection by P. graminis f. sp. avenae, a 52% reduction in yield was found compared to the treatment with fungicide application. This coincided with May et al. (2014), who recommended that the application of fungicide for the control of rusts in oats, should only be carried out in highly susceptible varieties. According to Murray (2007), the time of application of the fungicides is critical for the success in the control of the disease. Also, the treatments can be applied as treatments to the seed, mixed with fertilizers or sprinkled on the crop.

It should be mentioned that the percentage of loss of yield in some varieties of oats did not coincide with the percentage of susceptibility or damage caused by stem rust, such is the case of the Guelatao variety, which was one of the varieties most susceptible to rust. Stem, although it was not the most lost performance. The above coincided with Epstein et al. (1988) and Leyva-Mir et al. (2004), who mentioned that there are oat genotypes that are highly susceptible to infection by stem rust but that show an acceptable yield because of their high yield potential.

Days to flowering

The varieties with less days to flowering were Diamante R-31 (resistant to rust) and Parámo. This is important, because the earlier a variety is, in addition to choosing an appropriate planting time, it can reduce the risk of loss from stem rust (Smith, 1992). For this reason, the variety Diamante R-31 can be an alternative as a source of resistance if you want to make a cross with some variety of yielding oats but susceptible to stem rust.

The Opalo variety showed to be one of the later varieties in days to flowering and one of the most susceptible to stem rust, which indicates that this type of varieties is more difficult to escape from the attack of this phytopathogenic fungus, even and when the sowing dates are advanced (Figure 1). The flowering days allow us to choose the earliest varieties when the purpose of the production of these varieties is for forage, but when they are required for grain you need to know the days to maturity and thus calculate the planting date in which you can get rid of the attack of stem rust.

Figure 1 Days to flowering of 28 varieties of oats planted under storm in the high valleys of Mexico during the spring-summer 2013 and 2014 cycles. 

Days to maturity

It was observed that the variety Diamante R-31 was one of the varieties most resistant to rust, although its cycle was later compared to the earliest varieties (Figure 2), which behaved as highly susceptible, which indicated that the best way to control this disease is by generating oat varieties that contain horizontal resistance. Similarly, Cornide et al. (1993) mentioned that horizontal resistance is genetically polygenic and has as its main characteristic the lack of specificity before a series of races, which is why it delays the development of an epidemic or new race.

Figure 2 Days to maturity of 28 varieties of oats planted under rainy season in the high valleys of Mexico during the spring-summer 2013 and 2014 cycles. 

On the other hand, in the susceptible and early varieties, the yields will decrease unless they are sown in times where they manage to escape the attack of the rust, which will be the periods when this disease does not have the adequate conditions to develop and consequently severely damage the crop.


The best sowing dates for temporary oats were the dates of June 23 and 30, 2013 and 2014, since they were the dates with the lowest severity of stem rust caused by Puccinia graminis f. sp. avenae.

The variety of oats most resistant to stem rust in the 5 sowing dates evaluated was Diamante R-31, which is also early, so it is inferred that it can have minor genes of durable resistance. While, the varieties most susceptible to stem rust in the 5 planting dates were the varieties Tulancingo, Guelatao and Ópalo.

On the other hand, it was observed that the yield of oats in the presence of stem rust and without being controlled with any fungicide, severely decreases grain yield.

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Received: January 00, 2018; Accepted: February 00, 2018

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