1. Introduction
Wheat is a staple food crop, globally contributing 20% of the calories and proteins to the human diet [
1]. Thus, wheat is crucial for food supply and security in many countries around the world, and it is a critical part of the daily diet in West and Central Asia, and North Africa [
2]. In Tajikistan, wheat contributes significantly to food security through a variety of bread products made and in the preparation of a dozen types of different meals in various regions of the country [
3].
According to the World Food Program of the United Nations (WFP), a high proportion (30%) of the Tajik population is undernourished and about half of the population live on less then USD 1 a day [
4]. Similarly, the Food and Agriculture Organization of the United Nations (FAO) places Tajikistan among the countries where development goals targeting hunger are progressing slowly and where the prevalence of undernourishment is high (33%) [
5]. The ongoing COVID-19 pandemic may lead to significant increases in food prices, especially of wheat as a key product, and poverty levels in developing countries, including Tajikistan, may rise again [
6]. Food insecurity and poverty are the major reasons for several serious public health issues [
7]. Hence, the first important action to prevent severe health issues in developing countries like Tajikistan is to improve access for people to food, and especially to the staples. Thus, to ensure future food security in Tajikistan, sufficient wheat production in terms of quantity and quality is essential, together with sustainability in production to secure the environment.
Wheat production and yield of the crop are determined by a number of factors related to the choice of cultivar, the growing environment and cropping conditions. In Tajikistan, foliar diseases, poor seed quality with limited use of certified seeds, lack of appropriate crop management and weed control taking biodiversity into consideration, low availability of superior varieties to farmers, lack of financial investment and low level of farming knowledge among wheat farmers have been identified as major constraints on domestic wheat production and yield [
8,
9,
10]. Currently, sustainable weed control and certified seeds are two measures used to a limited extent, but with large opportunities to sustainably effect the wheat production and yield [
10]. Until now, some work has been carried out to improve seed quality through breeding for resistance to the main foliar diseases [
9,
11], while both weed management and seed-borne diseases have been handled limitedly. In a recent paper, weed management strategies that simultaneously focused on not hampering the extensive weed biodiversity in Tajikistan were discussed and propositions were made [
10]. Seed-borne diseases, which are transmitted to next generation of wheat through the seed [
12], are a major concern for Tajik wheat production, since farmers commonly use saved seeds without proper quality testing [
8,
10,
13]. Seeds can host a number of potentially pathogenic microorganisms [
14], and non-certified seeds or seeds from unknown sources have been shown to bear significantly higher levels of seed-borne diseases [
15]. Thus, to obtain high yields without the use of certified and resistant seeds would require the extensive use of chemical pesticide treatments. The major wheat seed-borne diseases are caused by fungi [
14]. A broad spectrum of fungi are present on the wheat seed, but the most important are common bunt (
Tilletia tritici (Bjerk.) Wint,
T. laevis Kühn) and loose smut (
Ustilago tritici (Pres.) Rostr.) [
16]. Furthermore, black pointed seeds are mainly known as a result of the presence of certain fungi on the seed [
10,
17]. In most countries worldwide, seed-borne diseases are strictly monitored, particularly within the grain industry [
18,
19], as well as in seed certification and seed movement [
20]. The breeding of resistant varieties contributes to sustainability in production as chemical pesticide measures can be reduced [
21].
Wheat is used for a range of products of which bread is known as the major one, which is also particularly true for Tajikistan. The bread-making quality of wheat is known to depend on many factors, and in particular, the genotype, the growing environment and the management practices are of importance [
22,
23]. Crop management practices such as nitrogen application, irrigation, soil conditions and management have been shown to affect both grain protein concentration and protein quality [
24,
25,
26,
27]. Earlier studies have shown a negative correlation between seed-borne diseases and yield, and a negative impact of specific seed-borne diseases, e.g., common bunt, loose smut, black point and Karnal bunt, on wheat grain and flour quality [
28,
29,
30]. Different protein fractions in wheat also affect bread-making quality [
31], e.g., there is a positive correlation between percentage of sodium dodecyl sulphate (SDS)-unextractable polymeric protein in total polymeric protein (%UPP), gluten strength and bread-making quality [
32,
33]. In Tajikistan and other similar countries, bread-making quality is essential in a food security perspective due to the importance of the bread in the daily diet of the Tajik people [
34].
The overall objective of the present study was to evaluate opportunities for sustainable wheat production with increased yield and quality to improve food security in a developing country such as Tajikistan. Thereby, the aims were to: (i) determine the magnitude, prevalence and pattern of fungi on wheat seeds and the presence of seed-borne diseases in wheat samples produced by farmers in Tajikistan; (ii) evaluate the protein quality of wheat produced by farmers in Tajikistan; and (iii) examine relationships and interactions between the presence of fungi on the seeds causing seed-borne diseases and protein quality in wheat produced by Tajik farmers. From the results on the seed-borne pathogens present and the defined bread-making quality, we elaborate on and suggest opportunities and a way forward for sustainable wheat production for food security. Furthermore, possible relationships between farm type, management, cultivation environment, quantity and quality of wheat production and the presence of fungi on the seeds and of seed-borne diseases in wheat produced by Tajik farmers were examined.
4. Discussion
The visual inspection of wheat fields on 21 farms in Tajikistan over two years revealed a generally low infection of common bunt (
Tilletia laevis and
T. tritici) and other seed-borne diseases. Despite this, grain samples from almost all farms investigated showed the presence of teliospores of both
Tilletia species, but predominantly
T. laevis. Moreover, the presences of other major fungi (e.g.,
Alternaria spp.,
Bipolaris sorokiniana,
Stemphylium spp., etc.) in the seed samples were also found. The majority of samples collected from the farms showed a significant level of black point symptoms, which could be either due to susceptibility of varieties grown [
51] or to late rain at the end of growing season, which enhances the disease [
52]. The findings in this study indicate that a high prevalence of wheat seeds infected with seed-borne diseases and the presence of fungi may lower the quality of Tajik wheat in terms of grain protein concentration and gluten strength, thereby threatening food security for the country.
The fact that common bunt was observed only in a few farms, although the teliospores were found in the majority of the seed samples, resembles results from previous studies in similar countries, e.g., in Syria common bunt was present in all wheat fields, but at a low level [
53]. Like common bunt, loose smut was only visually detected on few farms during the field survey. However, this may be explained by the fact that loose smut symptoms are visible at ear emergence, while the inspection in this study was performed later, during the flowering to dough stage. More than 20 other fungi species were isolated from the wheat samples. Some of these fungi are considered saprophytic, although they are known to cause damage in one of their life cycle phases, e.g.,
Penicillium spp. may cause decay in dry seeds [
50]. In addition, some saprophytic fungi are actually known to cause toxicity, i.e.,
Aspergillus spp.,
Rhizopus spp. and
Chaetomium spp. [
14,
54], and can become a serious health issue of human and animals from spoilt grain or feed [
54]. Species from the genera
Aspergillus,
Ulocladium,
Epicoccum and
Penicillium are also known to be allergenic for human and animals [
54]. In the present study, one of the main aims was to identify potential wheat pathogens. The following fungi species known to cause different diseases and damage in wheat were detected on grain samples:
Alternaria spp.,
Bipolaris sorokiniana,
Stemphylium spp.,
Curvularia spp.,
Cladosporium spp. and
Fusarium spp. Thus, on the basis of both sustainability reasons in production and for food security reasons, we suggest that wheat breeding should focus on increased levels of resistance towards fungi and pathogens in the wheat seed.
Alternaria spp. was present in the majority of the samples analyzed and was also predominantly present in samples showing black point symptoms (~87%). Previous studies have commonly found
Alternaria spp. in wheat seeds, but most have not observed any direct effect of this fungus on wheat quality [
55]. Many studies have identified
Alternaria spp. as one of the causes of black point [
56,
57,
58] as in the present study. Presence of the disease may become the reason for the degradation of commercial quality of wheat grain [
18,
59]. Some studies have also indicated a decrease in germination capacity in wheat seeds with black point [
60,
61], although contradictory results have been found in other studies [
58]. These contradictory results may be because different fungi can be present on wheat seeds showing black point, as found here. Khani et al. [
17] found out that two major factors for black point development are susceptibility of variety and environment conditions during the grain development period, such as higher humidity and lower temperature. Further studies of Tajik wheat genotypes under the various agro-climatic conditions will allow farmers to select the most desired ones to achieve a decreased rate or even complete elimination of black point wheat grains.
Farmers surveyed in this study admitted that the first action they take once any diseases appear is to use pesticides. However, serious issues are known to be caused from the misuse of pesticides, both towards the environment with contamination of soils and food [
62,
63,
64], but also on human health [
65]. On the other side, the quality of the available pesticides in the market is also not well controlled in Tajikistan. Therefore, farmers in Tajikistan and similar countries are to be trained in how to use environmentally friendly approaches of diseases management in wheat production. The use of resistant varieties and best crop management practices, including the use of certified seeds and crop rotation practices, are among the most sustainable measures to be taken here [
10].
Previous studies reported that a relationship was found between fungi on seeds and the protein quality of the grain [
66]. As was discussed earlier, in this study a negative relationship was found between several of the fungi present on seeds and TOTE (
Figure 4). TOTE is a known protein parameter correlating with grain protein concentration [
25,
67]. The same fungus correlated positively with %UPP, known to correlate with gluten strength [
24,
25]. However, there is generally a negative correlation between TOTE and %UPP [
68], which might explain some of the correlations with fungi observed in the present study too. In general, the protein quality of grain samples in the present investigation did not show very high TOTE or %UPP values. Although there was rather high variation in the different protein factors between the samples, the values were of similar magnitude as for the standard variety Dragon, a Swedish spring wheat variety with normal grain protein concentration (11–13%) and rather weak gluten quality [
31] that was used as a control in the SE-HPLC. The findings of relatively low protein content and gluten strength in Tajik wheat call for breeding activities to improve the yield and quality of local cultivars, which corresponds to breeding goals of the Tajik wheat breeding program to improve bread-making quality [
21]. A high proportion of Tajik wheat breeding material holds the high molecular weight glutenin subunits 5 + 10 [
69], and has a high grain protein concentration (unpublished results), offering good opportunities to achieve a better bread-making quality, thereby improving the food security. However, the issues with heterogeneity in the Tajik breeding material [
69] and the use of saved seeds by farmers [
13] need to be resolved for sustainable production of bread wheat in Tajikistan.
The present study evaluated possible effects of farm type, management and environmental factors such as elevation on the prevalence of seed-borne diseases and protein quality. Farm type was shown to have some impact on presence of fungi on wheat grain, with higher incidence of
Stemphillium spp. and
Curvularia spp. on grain from DF-type farms and of
B. sorokiniana on grain from PC-type farms. Variations in the presence of diseases between farm types could possibly be related to differences in production conditions, availability of machinery and use of various inputs. In general, the larger farms surveyed had more organized wheat production than the smaller-scale farms, as was also reported earlier [
10]. In particular, PC-type farmers knew the wheat variety they used, followed a crop rotation, used machinery for sowing and treated seed to control fungi. The positive correlation between knowledge of genotype grown and use of a crop rotation scheme corresponds with previous reports, as do the general findings on management in Tajik farms [
10]. Thus, the present study confirms the need of farmer education for sustainable wheat production in Tajikistan to obtain food security.
Land elevation played a minor role for presence of seed-borne diseases and for protein quality. In general, the wheat genotype mainly determines the quality of the grain [
26,
70]. However, in this study, the effect of the genotype could not be properly evaluated since the farmers surveyed, especially on DF-type farms, had limited knowledge of the genotype they were actually growing. Such lack of knowledge as related to the genotype grown has in a previous study been correlated to a lack of success in wheat production [
10]. Thus, human resource development (HRD) activities, such as training programs, are needed to educate farmers of all types in order to increase the success in wheat cultivation in Tajikistan. These should include formal training in schools, but also demonstration and dissemination of up-to-date information to farmers on sustainable crop production, including major diseases and weeds and opportunities, to improve the bread-making quality of wheat grain.
This study clearly showed that the health of homegrown wheat seeds in Tajikistan is rather poor, negatively effecting sustainable production and food security. Seed-borne diseases can be seen as a hidden threat to future sustainable crop production, with a negative impact on germination rate, number of normal seedlings and seed quality [
15]. Previous studies have shown that use of certified seeds of tested and accepted varieties leads to higher yield and financial income [
71]. A number of factors influence farmers’ willingness to use certified seeds, including knowledge level, financial capacity [
71] and most importantly, availability and trust in the certified seeds [
72]. Seed certification standards can help to control the spread of diseases, as certified seeds are usually free from pathogens causing seed-borne diseases [
15], thereby preventing major grain losses [
19]. Seed certification is currently not widely implemented throughout Tajikistan [
73]. Developments of a proper seed certification and seed health testing system would significantly contribute to higher yielding and more sustainable wheat crop production in Tajikistan and in other developing countries.