Influence of Agroclimatic Conditions, Life Form, and Host Species on the Species Complex of Wheat Septoria Pathogens

Abstract—Currently, Septoria is the basis of the pathogenic complex on wheat crops in Russia, occupying the predominant position among harmful fungal diseases. In case of severe wheat damage, the crop loss caused by the fungus Zimoseptoriatritici constitutes from 10–25 to 40–60%. Crop loss caused by the parasitizing of the fungus Parastagonospora nodorum ranges from 10–20 to 30–50% during the years of epiphytoty. The question of the economic significance of Parastagonosporaavenae has not yet been examined completely. However, depending on the area of wheat cultivation and the year of observation, its part in the Septoria population can reach 76.9%. It was of interest to study in detail the influence of the conditions of the specific year, life form, and species of wheat on the formation of the species composition of Septoria in the pathogenic complex of wheat. Among the complex set of factors included in the concept of the environment, a significant role belongs to its abiotic components, namely, climate and weather, but the variety as an environment-forming factor has a decisive role. Our studies were carried out in 2010–2017. During the research period, the weather conditions varied significantly over the years and were not always favorable for the development of plants and the formation of a good wheat crop. During the study, deviations from the long-term average annual values in the amount of precipitation during the vegetation period, and, in general, over the year, were noted. The years 2012, 2014, and 2015 were characterized by the highest moisture supply during the vegetation season. It has been shown that cooler days of April and May promote better development of P. avenae and P. nodorum. P. nodorum obtains its predominant development during the years with more humid weather within the vegetation period of wheat, in contrast to Z. tritici, which is more resistant to low humidity. These data demonstrate the adaptation of the pathogen to the conditions of an increased temperature regime and reduced amount of rainfall.


INTRODUCTION
The development of plant diseases is subject to fluctuations. This is manifested in a change in the distribution area in different regions and in the intensity of crop damage (Goodwin et al., 2015;Kuzdraliński et al., 2015;Ben Jabeur et al., 2017). These indicators determine the size of the crop shortfall and the amount of economic damage (Goloshchapov, 2011;Schilly et al., 2011).
Among the complex set of factors included in the concept of the environment, a significant role belongs to its abiotic components, i.e., climate and weather, however, a decisive role remains with the variety as an environment-forming factor (Simón et al., 2007;Torriani et al., 2009;Sanin, 2013;Sklimenok and Buga, 2014;Evseev, 2015).
Since 2000, the authors of this article have been studying the species composition of the Septoria disease on the cultivars of winter and spring wheat in the territory of the Central Black Soil Region (Tambov, Lipetsk, Voronezh, Kursk, and Belgorod regions). It was of interest to study in detail the influence of the conditions of the year, life form, and species of wheat on the formation of the species composition of Septoria in the pathogenic complex of wheat (Plakhotnik et al., 2007;Zeleneva andSudnikova, 2017, 2019;Zeleneva et al., 2018).

MATERIALS AND METHODS
The studies were carried out in the period 2010 to 2017. To study the relationship between the frequency of Septoria species and the agroecological conditions prevailing in different years, infectious material was collected on production crops and state variety plots, as well as from the collections of research institutes from sixty cultivars of soft winter wheat (Triticum aestivum L.), thirty-three of soft spring (Triticum aestivum L.), and sixteen of durum spring wheat (Triticum durum Desf) in five regions of the Central Black Soil Region (CBSR) (Tambov, Lipetsk, Voronezh, Kursk, and Belgorod regions).
Mycological experiments were carried out in specially equipped rooms. To determine the species composition, the collected samples were examined under the microscope. A small piece (5 × 5 mm) of the affected tissue with fruiting bodies was placed on a slide into a drop of water, covered with a cover slip, and examined at low magnification. After some time, the release of pycnospores was observed. The type of the pathogen was determined by the shape and size of the spores emitted (Pakholkova et al., 2008). There were at least 50 samples from each specimen.
Based on the data obtained, the frequency of certain species of Septoria was established (Pakholkova et al., 2017) according to the formula: where N is the frequency of the species, %; A is the number of cases in which the given species of Septoria was noted; and B is the total number of cases in which both this species and others were encountered.
The influence of agroecological conditions on the incidence of pathogens of wheat Septoria disease was determined using Fisher's F-test. The critical level of significance when testing statistical hypotheses (p) was taken equal to 0.05.
To carry out multiple comparisons of the mean values characterizing the frequency of Septoria species in different years of the conducted studies, we used the Bon-

100, N A B
= × ferroni test. The critical level of the significance of differences was taken as p = 0.05/number of comparisons. Statistical data processing was performed using the STATISTICA computer program.  Fig. 1.

RESULTS AND DISCUSSION
The abnormal weather conditions of 2010 with a high temperature regime and air and soil drought adversely affected the host plant and the pathogenic complex. Low development of Septoria blight on wheat was noted; however, the species Z. tritici had the highest frequency in the pathogenic complex of Septoria blotches: 96.71%. P. avenae and P. nodorum in 2010 had the lowest frequency for the entire study period (0.6 and 2.69%, respectively).
As shown earlier, Z. tritici was the most abundant Septoria species throughout the years of study in Tambov region. According to the generalized results of the analysis of the frequency of Septoria species on wheat, it was shown that the frequency of the species Z. tritici in 2011 amounted to 72.58; in 2015, 86.5; in 2016, 82.37; and in 2017, 81.08%. The years 2012, 2014, and 2013 should be highlighted separately. They were characterized by the most favorable agroecological conditions for the development of the species Z. tritici. Its frequency exceeded 90 cases out of 100 and amounted to 90.08, 90.16, and 92.42%, respectively.
In terms of the frequency, over eight years of study, P. nodorum occupied a stable second position in the pathogenic complex of Septoria spots. In 2013, its indicator was 4.97; in 2014, 7.59;and in 2012and in , 7.68%. In 2015and in , 2016, the frequency of P. nodorum exceeded 10% and amounted to 10.04, 11.97, 14.08, and 15.2%, respectively. P. avenae is a rare species. It usually stands out at the late stages of wheat development, and therefore, does not harm the quality and quantitative indicators of agricultural products. Its frequency in 2012, 2013, and 2014 did not exceed 3%. In 2016, the indicator was 6.56%; in 2017, 9.67%; and in 2011 the frequency exceeded the threshold of 10% and amounted to 11.84%.
The influence of agroecological conditions that have developed over the course of eight years of study on the frequency of the species Z. tritici , P. nodorum, and P. avenae was determined using Fisher's F-criterion (Table 1). According to Fisher's criterion, the influence of agroclimatic conditions on the frequency of all three species of Septoria was revealed. The conditions of the year influenced particularly strongly the frequency of the species Parastagonospora nodorum (Fisher's F test = 11.93).
A weak positive correlation was found between the frequency of Z. tritici and the average temperature in April (0.22) and May (0.13) ( Table 2). An inverse weak correlation was found between the frequency of P. nodorum and P. avenae and the temperature in April (-0.167 and -0.233) and in May (-0.109 and -0.100, respectively). It follows that the warm temperature regime in May and April has a positive effect on the frequency of Z. tritici, while the cooler days of these months promote a better development of P. avenae and P. nodorum.
There is a weak negative correlation between the frequency of Z. tritici and the humidity in April and June and the average for four months (-0.097, -0.117, and -0.090, respectively). It should be noted that there is a weak direct relationship between the frequency of P. nodorum and humidity in April (0.089), June (0.116), and the average indicator for four months (0.092). The data given in Table 2 show that P. nodorum receives predominant development in the years with more humid weather during the growing season, in contrast to the species Z. tritici, which is more resistant to low humidity.
The obtained results of the analysis of variance of intergroup differences in the frequency of different species of Septoria are given in Tables 3, 4, and 5.
Between the compared indicators of the frequency of the species Z. tritici, P. nodorum, and P. avenae on wheat cultivars in the different years of study, there are differences at the accepted level of significance between the indicators of 2010 and all other years of research. As noted above, this year was characterized by abnormally hot conditions, a low amount of precipitation (in some places none at all), and soil and air drought.
The conditions of 2011 also affected the frequency of the species Z. tritici and P. avenae . The conditions of 2011-2012, 2013, 2014, 2015, and 2016 were significantly different, influencing the frequency of the species (Tables 3, 4). With regard to the frequency of P. nodorum in 2011, there are differences from 2012, 2013, and 2014 (Table 5).
There were significant differences in the frequency of P. avenae in 2014 and 2017 (Table 3).
Such differences are associated with significant changes in the weather conditions during the study. Thus, the most moisture-secured were the years 2012, 2014, and 2015 (Table 3). The year 2011 was characterized by cool weather and a decrease in precipitation during the spring-summer months. In 2017 the precipitation dropped even less (312 mm) than in 2011 (396 mm); however, the differences in the frequency    However, it appears that, in this case, the overwintering of the pathogen and differences in climatic characteristics of the preceding winter months, March and April, were essential. Differences were registered in the frequency of Z. tritici, isolated from the infectious material in 2012-2017, 2013-2016, 2013-2017, and 2014-2017 (Table 4).
Thus, despite the fact that the agroclimatic conditions of the year have an impact on the frequency of Z. tritici, P. nodorum, and P. avenae, the differences established using the Fisher's F-criterion (Table 4), were, apparently, influenced by the indicators of 2010 and 2011. In other years, no significant differences were found for the species P. nodorum and P. avenae (Tables 6, 8). For Z. tritici, in addition, there were differences in the frequency isolated from the infectious material in 2012-2017, 2013-2016, 2013-2017, and 2014-2017 (Table 7).
Analyzing the results of the dependence of the frequency of Septoria species on the life form and wheat species (Fig. 2), it can be noted that no significant effect was found. All life forms of wheat are affected by the three species of Septoria with the same pattern. The frequency of the species Z. tritici during the research period varied from 79.77% in the durum spring wheat to 86.26 and 88.49% in soft spring and winter wheat, respectively.
The frequency of P. nodorum on the cultivars of soft winter wheat was 8.18% and on soft spring wheat cultivars, 8.99%, and on the cultivars of durum spring wheat, the indicator exceeded 10% and amounted to 14.53%. P. avenae was recorded more often on the cultivars of soft winter wheat. Its frequency was 9.98%. Less commonly, this species affected the cultivars of soft and durum spring wheat: 4.82 and 5.90%, respectively.
The impact of life forms and species of wheat on the frequency of Z. tritici, P. nodorum, and P. avenae were determined using Fisher's F-test. The critical level of significance when testing statistical hypotheses (p) was taken equal to 0.05 (Table 6).
According to Fisher's F-criterion, the life form and species of the host plant significantly affect the frequency of the species Z. tritici and P. nodorum (F-criterion = 8.71 and 2.00, respectively). This method did not reveal the influence of life forms and wheat species on the frequency of P. avena.
Using the Bonferroni test, a pairwise comparison was made of the average frequency of different Septo-ria species, depending on the life form and species of the host plant. The results are presented in Tables 7, 8, and 9.
The use of this statistical method made it possible to establish significant differences in the frequency of P. avenae on soft and durum wheat and no differences when comparing the frequency of the species isolated from soft winter and spring wheat.
A similar tendency was observed in relation to the frequency of Z. tritici on the cultivars of soft winter, soft spring, and durum spring wheat in pairwise comparison. Differences between soft and durum wheat cultivars were noted. When comparing the frequency of P. nodorum species depending on the life form and species of the host plant, significant differences were established between soft winter wheat and durum spring wheat, but no differences between soft and durum spring wheat or soft winter and spring wheat were found.

CONCLUSIONS
Using Fisher's F-criterion and the method of pairwise comparison with the Bonferroni correction, a significant effect of agroclimatic conditions of the year, life form, and type of formation of the species composition of the Septoria wheat spot was shown.
The indicators of the correlation coefficients made it possible to establish that warm temperatures in May and April have a positive effect on the frequency of the species Z. tritici. The average temperature in April for eight years of study was +12.39°C, and the average temperature in May was +21.73°C. It was shown that the cooler days of April and May contributed to a better development of P. avenae and P. nodorum. Based on the analysis of the correlation coefficients between the frequency of the occurrence of Septoria species and the indicator of average humidity, the conclusion can be made that P. nodorum predominantly develops in years with more humid weather during the vegetation season of wheat, in contrast to the species Z. tritici, which is more resistant to low moisture.