Northern Himalayan Region of Pakistan with Cold and Wet Climate Favors a High Prevalence of Wheat Powdery Mildew

W being the most important food crop of Pakistan, remains the strong component of national food security. High wheat production in Pakistan is threatened by wheat diseases, particularly rusts and powdery mildew. Both rusts and powdery mildew are obligate parasites causing important wheat diseases like leaf/brown rust (LR) caused by Puccinia triticina, yellow/stripe rust (YR) caused by P. striiformis, stem/black rust (SR) caused by P. graminis f.sp. tritici and powdery mildew (PM) caused by Blumeria graminis f.sp. tritici. Although several efforts have been made to assess the prevalence of rusts on wheat varieties, limited information is available on the distribution of powdery mildew in various wheat growing regions of Pakistan.

and early 1990's, prevailing in many wheat fields, with further sporadic prevalence associated with favorable climatic conditions. During early 2000 the disease prevailed again wherever the wheat is cultivated in the country in humid and sub-humid areas (Rattu et al., 2009). Powdery mildew of wheat has also worldwide distribution and is especially important in areas with cool and dry climates, including China, Europe, and South America (Dubin and Duveiller et al., 2011). It was considered as devastating disease in northern Europe where cool and mild climate prevails, leading to damage of grain yield and quality (Morgounov, 2012). The disease occurs more frequently in wheat growing areas with a moist environment. The disease is favored by cool and humid weather with optimal temperatures ranging from 15°C to 18°C and with relative humidity ranging from 75-100%. Such conditions are more prevalent in the northern Himalayan region of Pakistan. The growth of pathogen is negatively affected by temperatures above 25°C, leading the disease progression to slow down as the growing season progresses into the hotter months (Leath and Bowen, 1989). In recent decades, this disease is becoming of more importance even in areas with warmer and drier regions because of intensive production with higher plant densities, replacement of long by semi dwarf varieties, nitrogen fertilizers, and irrigation (Cowger, 2016). The high prevalence at the time of grain filling or earlier could lead to impart substantial losses on wheat crop. Commercial yield losses due to powdery mildew in Western Europe are usually below 10%, with the maximum 20% losses in the United Kingdom. The reported yield losses in North Carolina ranged between 5-17%, generally 10 to 15% in Russia but sometimes reaches up to 35%,up to 62% in Brazil,and 30 to 40% in China under severe epidemics (Mehta, 2014). The yield reductions of higher than 40% are unusual, but infections at early stage may lead to the complete loss of seedlings or tillers ultimately failing to produce seeds (Cunfer, 2002). In areas of high disease prevalence, the disease may impart significant yield reductions, which needs to be controlled to avoid economic losses.
Various practices including agricultural and chemical controls have been utilized to reduce the effect of diseases, but increasing production costs, polluting the environment and encouraging the speedy evolution of new pathogen races (Hardwick et al., 1994;Parks et al., 2008;Ryabchenko et al., 2003). Host resistance is the only cost effective and economical way to restrict the disease (Huang et al., 2000;Huang and Röder, 2004). Genes conferring resistance against powdery mildew are known as Pm genes. Sixty Pm genes have been identified, formally named as Pm1 to Pm50, and some other temporarily designated genes (McIntosh et al., 2012;Mohler et al., 2013;Xiao et al., 2013). Wheat genetic background narrowed with the passage of time by selecting high yielding wheat varieties with more homogeneous genetic backgrounds throughout the world, and replacing highly variable landraces leading to unpredicted challenges in resistance breeding ( Johnson, 1992;Gupta et al., 2010;Muhammad et al., 2011;Karsai et al., 2012). The effectiveness of these powdery mildew resistance genes has been reduced with the passage of time owing excessive deployment of single resistance genes with race-specific nature (Xiao et al., 2013). Therefore, it is mandatory to continuously identify and transfer new and effective sources of powdery mildew resistance into improved wheat germplasm to counter the continuous evolution of virulence in powdery mildew pathogen. However, it could only be attained to identify the relative prevalence of powdery mildew across location of Pakistan in major wheat growing regions and the status of various wheat varieties grown in the powdery mildew hot spot regions.
In the past, breeding programmes in Pakistan has little consideration to utilize powdery mildew resistance in improved genetic stocks and thus genetic improvement of wheat varieties against powdery mildew was limited. This was mainly due to little information on distribution of the disease and the regional risks of epidemics across Pakistan. During the present study a countrywide surveillance effort was made to (i). identify the relative distribution of powdery mildew across the country and (ii). assess the status of powdery mildew infection on various wheat varieties grown in powdery mildew prone areas.

Materials and Methods
Wheat powdery mildew surveillance was carried out in major wheat growing areas of Pakistan during the year 2016, 2017 and 2018 ( Figure 1). The surveillance was carried out in mainly farmer fields and to some extent at research institutes and stations, all under natural field conditions. Surveillance activities were carried out from March to July starting from southern part of the country and ending in the north, spanning mainly from heading to grain filling duration. A total of 1211 fields were surveyed during the three years from different locations of Pakistan. Disease scoring Evaluation of disease was based on foliar infection. For scoring powdery mildew, two parameters were taken in consideration i.e., host reaction and disease severity, which was recorded on leaves of each wheat variety in a field (Ali and Hodson, 2017). Modified Cobb scale (0-100 scale) was used to estimate disease severity and percentage of infected tissue of plant in a field (Peterson et al., 1948), while considering the overall field infestation.

Analyses of data
The surveillance data was analysed in MS Excel and in R-statistical environment. The disease status was analysed in relation to provinces, districts and host varieties. The geographical distribution of the powdery mildew across various geographical locations and different hosts was analysed based on its relative prevalence as a function of geography and host.

Results and Discussion
Surveillance of powdery mildew disease allowed to measure the relative importance of disease at regional and country level. An overall low powdery mildew was detected in the southern half of Pakistan, while its prevalence was high in the northern Himalayan regions of Khyber Pakhtunkhwa and Azad Jammu and Kashmir.

Surveillance details
Surveillance enabled to assess the relative distribution of powdery mildew across locations and the status of different varieties in different geographical regions. Surveillance was carried out in 63 districts during 2016, 69 districts during 2017 and 34 districts of Pakistan during 2018 (Table 1 and Figure 2). A total of 1211 wheat fields were surveyed during three years. In AJK 27 fields, Baluchistan 4 fields, Gilgit-Baltistan 15 fields, Khyber Pakhtunkhwa 516 fields, Punjab 396 and Sindh 253 fields were surveyed over three years (Table 2).

Relative distribution of powdery mildew across locations
The powdery mildew incidence and severity varied over the two years, across provinces and districts. Significant levels of powdery mildew were observed at most of the locations in northern KP surveyed during 2018 followed by wheat season of 2017, however, a lower disease pressure was observed during 2016 (Table  3). A total of 51 fields out of 1211 fields had a high disease pressure with a powdery mildew severity score of 40 and above (Table 4). In 2016, 8 fields were recorded with high powdery mildew severity out of total 437 field surveyed. While in 2017, 13 fields were recorded with high powdery mildew severity out of 480 fields and during 2018, 21 fields were recorded with high severity out of 294 total fields surveyed (Table 3). In AJK, three fields in Hattian Bala and Muzzafarabad districts were recorded with high powdery mildew severity in 2016 and 2017. In KP, the maximum numbers of fields with high disease severity was observed in district Mansehra (10 fields), followed by Dir Lower (9 fields) and Dir Upper (8 fields) over three years. In Gilgit-Baltistan, in five fields powdery mildew was detected with only one field with high severity. The number of fields with high disease severity in other districts of Khyber Pakhtunkhwa ranged from one to five. In Punjab, powdery mildew severity was observed in Rawalpindi, Bhakar, Mandi Bahaudin, Hafizabad and Chakwal districts, while in Sindh none of the field was infected with powdery mildew disease ( Table 4).

Status of host varieties against powdery mildew infection
Powdery mildew incidence varied on different hosts across different locations. The disease was observed on many varieties in KP, where wheat fields with varieties PS-2005, Shahkar and some unknown lines were observed with high disease severity over three years. In 2016 and 2017 high disease was observed on Galaxy-13 along with some local lines, while on Faisalabad-08 and PS-2008, the disease was observed only during 2016. The maximum numbers of infected fields were recorded for Galaxy-13 followed by Shahkar. In AJK and Punjab, only some local and unknown varieties were recorded with powdery mildew (Table 5). Powdery mildew is an important disease of wheat and cereals with a worldwide distribution, but the disease is of significant importance in regions with dry and cool climatic conditions, including China, Europe, and the Southern areas of South America (Dubin and Duveiller et al., 2011). In recent decades, this disease is becoming more prevalent even in areas with warmer and drier climates because of extensive use of nitrogen fertilizers, intensive production with higher plant densities, and irrigation (Cowger et al., 2012). Its global frequency remained stable over time, but increased by 10% in the last 10 years in Central and Eastern Europe (Morgounov et al., 2012). Relatively cold environment and high humidity favors disease development ( Jones and Clifford, 1983;Wiese, 1987), which was the case in the present study, the disease was more prevalent in cold and humid areas.
Powdery mildew was dominated in the cool areas of Pakistan, particularly the Himalayan region, which could be attributed to the prevalent weather conditions, which favors successful establishment of the disease. Temperature ranging between 12°C to 20°C with average temperature of 16°C in wheat season would result in damaging epidemics of powdery mildew (Te-Beest et al., 2008). Our results are also in broad agreement with previous reports of the optimal temperature which suggested range for mildew between 15°C and 22°C ( Jones and Clifford, 1983;Wiese, 1987). On contrary, the disease was absent in the warmer areas of Sindh and Punjab. Only in Rawalpindi division, powdery mildew was observed with few locations which could be attributed to the favorable microclimate developed during rainfall in vigorous crops with high fertilize application (Cowger et al., 2012).
High rain falls enable to maintain desirable humidity for powdery mildew infestation, which occurs in the Himalayan regions of Pakistan, creating good conditions for powdery mildew development. This high humidity is also absent in the southern part of the country, resulting in low powdery mildew infestation ( Jones and Clifford, 1983;Wiese, 1987). Thus, in the northern part, the prevalent high humidity and cold climate would be responsible for the onset of disease ). Seasonal variability in temperature and humidity could result in differential onset of various diseases (de Vallavielle-Pope et al., 2012). Powdery mildew dominated in cold regions all the three years, with a slight increase in frequency of powdery mildew during 2017 as compared to 2016. This seasonal variability in the Himalayan region could be attributed to the cool and mild climatic conditions of the area.

Conclusions and Recommendations
This study concludes that wheat powdery mildew is emerging as potential threat to high yielding of wheat especially in northern part of the country. The disease incidence fluctuated oven the surveyed years. No disease was observed in the Sindh and was absent at maximum locations in Punjab because of the relatively high temperature during wheat season in those areas. The disease incidence was also low in southern KP, while in Northern KP and AJK where cool and humid climatic conditions prevail, the disease was more prevalent. Severe infestation was observed on some wheat varieties i.e., Galaxy-2013, PS-2005, Faisalabad-2008, Shahkar and some local lines, mainly deployed in those areas. The information should be considered while breeding wheat for genetic resistance against major diseases, particularly in breeding programmes for northern part of the country.