Prior to this study, pathogenic variability of Bgh populations has been investigated in a number of countries around the globe [17,18,19,20,21,22,23]. However, the virulence structure of Bgh populations in Kazakhstan and other countries in Central Asia (Uzbekistan, Turkmenistan, Kyrgyzstan, and Tajikistan) was still unknown. This study characterized the virulence structure of Bgh populations in barley-growing regions of Kazakhstan and identified pathotypes of Bgh and the frequency of their occurrence in two regions of Kazakhstan. To the best of our knowledge, this study represents the first documentation of the virulence structure of Bgh in Central Asia.
Based on 107 isolates collected during a 2 year period, 23 pathotypes with virulence complexity ranging from 1 to 6 were identified (Table 3). Two pathotypes, 24 and 64, were identified to be of importance in the barley production in Kazakhstan due to their occurrence across the entire study area. They differ only by one virulence gene, i.e. pathotype 24 is avirulent to gene Mlk, and pathotype 64 is virulent. In Kazakhstan all tested isolates were avirulent on lines with genes Mla9, Mla1 + MlaAl2, Mla6 + Mla14, Mla13 + MlRu3, Mla7 + MlNo3, Mla10 + MlDu2, Mla13 + MlRu3, Mlo-5 and virulent on the line with gene Mla8 (Table 1). Frequency of isolates virulent to genes, Mlg + MlCP and Mla12 + MlEm2 was very low. In some populations (Saryagash, Tulkubas, Ordabasy) isolates virulent to genes Mla22 and Mlat were detected at frequency of 11.1–33.3%. The isolates virulent to these two genes occurred frequently in European, Australian [19] and South African populations [21]. It has been recently reported that line P12 [10] with gene Mla22 is the most useful differential cultivar, i.e. possesses the maximal pathogen differentiating ability. However, none of commercial barley varieties includes this gene [20]. In our experiments isolates virulent to genes Mla3, Mlg + MlCP, Mla12 + MlEm2, Mla22 and Mlat were found only in some areas of South Kazakhstan region where winter varieties of barley are cultivated. In total virulence diversity of Bgh pathotypes was much higher in populations on winter barley varieties versus spring barley. It has been shown previously that the virulent pathotype (Va22) to gene Mla22 occurs only on winter barley varieties in France and fails to infect spring barley [25]. In central Europe, winter barley is infected by a broader spectrum of pathogens than spring barley and powdery mildew fungus is dominant among them on susceptible cultivars [26]. Moreover, Bgh pathotypes virulent to many resistance genes including genes Mla3, Mlg + MlCP, Mla12 + MlEm2 и Mlat were detected just on winter barley varieties [27]. According to Dreiseitl and Kosman [21] directional selection might be responsible for an increasing virulence frequency to resistance genes Mla12 + MlaEm2, Mlg + MlCP, and MlLa, which may be present in some varieties. Confinement of the most virulent pathotypes (72, 60, 57) to winter varieties of barley (Yuzhno-Kazakhstanskiy 43 and Bereke 54) could sufficiently effect the progress of an epiphytoty, particularly in the areas where these cultivars cover considerable acreages. There is also possibility of their future occurrence and spread on commercial varieties of spring barley. Therefore any strategy based on major resistance genes must incorporate two or more of the following genes Mla9, Mla1 + MlaAl2, Mla6 + Mla14, Mla13 + MlRu3, Mla7 + MlNo3, Mla10 + MlDu2, Mla13 + MlRu3. By present many interesting findings on sources of resistance genes to barley powdery mildew have been published worldwide. Postulation of resistance genes to powdery mildew of barley is a major method of their identification in barley varieties. For instance, some researchers [1, 2, 24, 26, 28] postulated Ml-genes in winter and spring barley varieties by this method. Among them the following barley varieties are of particular interest for breeders in Kazakhstan: Algerian (Mla1) [1], Agra, Arve, Thule (sources of gene Mla9) [2, 28], Shamu, Baronesse (sources of gene Mla3) [2], Atlas (source of gene Mlat) [1], Kristaps, Rasa (sources of genes Mla7, MlNo3, Mlg) [28]. They are carriers of effective resistance genes to Kazakhstanean Bgh isolates. Besides experience from Europe suggests the best ways of achieving durable resistance is to use either mlo [29] or combinations of minor genes. The recessive resistance gene mlo has remained effective for more than 50 years and is the mainstay of mildew control in European winter barley plantings [5].
Minimal intrapopulation diversity judging on all statistical indices (H
W
, H
G
, D) was displayed by the population from Zhambyl region, and maximal one by the population from South Kazakhstan population (Table 5). The results of the study show significant difference even within the limits of one host variety. Spring barley variety Baisheshek is a source of infection in some areas of South Kazakhstan and Zhambyl regions (Table 2). Analysis of pathotype structure of the fungus isolated from this cultivar showed higher virulence diversity of South Kazakhstan isolates versus Zhambyl isolates. Since there is no information on resistance genes in commercial barley varieties it is impossible to assess reliably which genes could influence the results of the virulence analysis. Powdery mildew in Kazakhstan is mainly an infection that is introduced from other countries, so one of the factors causing this difference could be different ways of the colony migration. Primary infection could be brought into South Kazakhstan region by airflows from adjacent Central Asian countries (Uzbekistan, Tajikistan), and into Zhambyl region by airflows from Kyrgyzstan and China. Virulence of the pathogens from Zhambyl population actually does not differ from that of the isolates from Chinese population [22], and the structure of Bgh populations in Uzbekistan and Tajikistan is still not known. The greatest virulence polymorphism of isolates was observed on lines with genes Mlra, Mlk, MlLa and Mlh (from 10.0 to 78.6%).
The data of many studies show that the virulence of the barley powdery mildew pathogen differs greatly in different eco-geographical regions. For instance, Czech population demonstrates high phenotypical diversity and the lowest mean complexity of virulence versus Israel population [18]. Virulence of Chinese Bgh populations differs substantially from the same of European populations; the only similarity consists in virulence to genes Mla8 and Ml(Ch) [22]. It has been recently shown that the structure of Bgh populations in South Africa is very variable, contains unique virulence frequencies and associations and differs from populations in other parts of the globe [21]. Comparison of our own results with published data displays low similarity of populations in Kazakhstan to European, African, Australian and South-West Asian populations. Particularly, the virulence rate of Bgh populations in Kazakhstan is much lower than in Europe [19, 20], South Africa [21] and South-West Asia [18]. The difference between Kazakhstanean and Chinese populations consists mainly in the fact that the pathogens isolated in South Kazakhstan are virulent to some effective resistance genes (Mla3, Mlat, Mlg, Mla22) in China [22]. The Australian population also differs from population in Kazakhstan, because the population of Bgh in our country contains the isolates virulent to gene Mlra that is effective in Australia [5].