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The necrotrophic fungus Pyrenophora tritici-repentis is the causal agent of tan spot of wheat, also known as yellow spot. Tan spot is one of the main foliar diseases of wheat, responsible for significant yield loss worldwide. To improve tan spot management, genetic control has been investigated and resistance in some cultivars improved; however, the complexity of the pathosystem wheat - P. tritici-repentis makes integrated disease management strategies very important. In this chapter, we provide an overview of the current state of knowledge of tan spot, including a basic understanding of characterization, pathogenicity, population biology, the global distribution of races, and the genetics of the wheat - P. tritici-repentis interaction. Furthermore, we describe several strategies that can be employed to control tan spot including, seed sanitation, cultural practices, fungicide and biological controls, as well as complementary alternative measures such as fertilization for efficient disease management in wheat production systems.
Agricultural Sciences, Natural Resources and the Environment Faculty, Laboratory of Phytopathology, Bolivar State University, Ecuador
Eliseu Maciel Faculty of Agronomy, Crop Protection Department, Laboratory of Plant Pathogen Interaction, Federal University of Pelotas, Brazil
Hadley Randy Kutcher
Crop Development Centre/Department of Plant Science, University of Saskatchewan, Canada
Leandro José Dallagnol*
Eliseu Maciel Faculty of Agronomy, Crop Protection Department, Laboratory of Plant Pathogen Interaction, Federal University of Pelotas, Brazil
*Address all correspondence to: leandro.dallagnol@ufpel.edu.br
1. Introduction
Wheat is the most important crop in the world in terms of consumption. Diseases and insect pests cause yield losses of approximately 21.5%, estimated at a global level, therefore affecting food security [1]. Tan spot caused by the necrotrophic fungus Pyrenophora tritici-repentis (Ptr) is one of the most important diseases of wheat worldwide. This disease is increasingly recognized as an important leaf disease on wheat that causes yield losses up to 50% [2, 3, 4, 5]. Since the first report of the pathogen in Japan in 1928, Ptr has been reported in almost all continents, indicating its wide geographic distribution [6, 7]. Over the past three decades, tan spot has become increasingly important, and its prevalence is associated with frequent wheat production in crop rotations or monocropping and cultivation of susceptible wheat genotypes [8, 9]. High yield losses and reduced seed quality occur when the pathogen infects plants during the booting and flowering growth stages [10, 11].
In this context, efficient and sustainable disease management tools are needed to maintain wheat production [1]. Hence, a combination of strategies has been tested to reduce the damage caused by Ptr; these strategies include chemical, cultural, genetic, and, sometimes, biological control [12, 13, 14]. A considerable amount of data has been published on chemical control and cultural practices. These studies have contributed to the management of the disease worldwide, particularly when sources of resistance are unavailable. Despite this, to improve tan spot management, the genetics of resistance has been investigated to develop less susceptible germplasm [15, 16]. For this, research has been conducted to understand the host-pathogen interaction, as well as the pathogen race structure worldwide. Furthermore, other complementary strategies for tan spot management have been studied for the disease control such as the use of fertilization. Recent studies have demonstrated that some mineral elements such as nitrogen (N) and silicon (Si) contribute to reduce tan spot damage [17, 18, 19].
Therefore, the aim of this chapter is to provide the current knowledge of pathogen characterization from the general aspect of the disease cycle, the global distribution of pathogen races, and genetics of the wheat-Ptr interaction to understand the basic aspects of genetic control. Also, we describe management strategies for pointing out the possibilities of new alternatives for efficient management of tan spot.
2.1 Fungal taxonomy and morphological characterization
The causal agent of tan spot in wheat belongs to:
Domain: Eucaria.
Kingdom: Fungi.
Phylum: Ascomycota.
Class: Dothideomycetes.
Order: Pleosporales.
Family: Pleosporaceae.
Genus: Pyrenophora.
Species: Pyrenophora tritici-repentis.
Pyrenophora tritici-repentis (Died.) Drechsler is used globally for the fungal sexual state while Drechslera tritici-repentis (Died.) Shoemaker for asexual state [20, 21]. Sexual reproduction of Ptr includes the formation of pseudothecia containing ascospores in asci [22]. Pseudothecia are black, spherical to subspherical, beaked, and 200 to 325 μm in diameter [23]. The beak supports a number of dark-brown sterile setae near the ostiole [24]. The asci are bitunicate and separated by pseudoparaphyses, with a length of 195 to 220 μm, containing eight ascospores [23]. The ascospores are brown, oval to globose, contain three transversely oriented septa, multinucleate, and range in length from 40 to 70 μm and in width from 18 to 25 μm [23]. The center cell of an ascospore has a longitudinal septation of four to five cells [22, 24]. Asexual reproduction includes the formation of erect conidiophores, up to 250 μm long and simple with a swollen base that gives rise to conidia that are subhyaline, cylindrical, typically four to seven septa, and multinucleate with conically tapered basal cells [24]. The conidia range in length from 117 to 218 μm and in width from 16 to 18 μm [25].
2.2 Life cycle
Following the crop harvest season, Ptr can survive on infected wheat stubble as mycelium or as pseudothecia [26, 27]. In the next season, mature pseudothecia release ascospores as soon as wheat is sown, which serve as the primary inoculum that infects young plants (Figure 1). Ascospore release can continue through the crop season and is favored by rainfall or high relative humidity and temperatures >10°C [28]. Additional sources of primary inoculum include infected seed, conidia on infested crop residues, volunteer wheat plants, and alternative grass hosts (Figure 1) [29, 30, 31].
Figure 1.
Cycle of host–pathogen relationship of wheat tan spot caused by Pyrenophora tritici-repentis. The pathogen overwinters on wheat straw, infected seeds, and on alternative hosts. On wheat straw, the fungus may produce pseudothecia with ascospores and conidia. When weather conditions are conducive, mature ascospores and asexual conidia are released that serve as primary inoculum to infect young plants. Mature lesions produce new conidia that serve as secondary inoculum throughout the growing season and are dispersed by wind and rain promoting infection of new plants or reinfection. Plant infection may lead to pathogen infection in the seeds, as well as increase the amount of infected crop debris in the area, increasing the primary inoculum for the next season. Photo credits by Andrea Román and Leandro José Dallagnol.
Several plant species can serve as alternative hosts to Ptr such as triticale (× Tritico secale), barley (Hordeum vulgare), and rye (Secale cereale). Other grass species may also be hosts such as Siberian wheatgrass (Agropyron sibericum), sand bluestem (Andropogon hallii), meadow brome (Bromus biebersteinii), sheep fescue (Festuca ovina), June grass (Koeleria cristata), little bluestem (Schizachyrium scoparium), green foxtail (Setaria viridis), needle and thread (Stipa comata), and tall wheatgrass (Thinopyrum ponticum) [32].
After infection by the primary inoculum, mature lesions on leaves are the main sources of conidia, and this secondary inoculum plays an important role in the progress of the tan spot epidemic during the growing season (Figure 1) [6]. Conidia are produced on wet leaves in the dark and dispersed by wind and water splash, resulting in the infection of new plants and plant reinfection [33, 34]. Infection can occur on leaves, stems, and spikes (Figure 2) [30]. The latent period ranges from 3 to 6 days after conidia are deposited on host tissue, depending on the resistance of the cultivar and weather conditions [35, 36, 37].
Figure 2.
Debris from a previous wheat crop serves as the inoculum source (conidia and ascospores), which infect young wheat leaves. Increased number and size of lesions on young plants increase the amount of secondary inoculum, thereby accelerating epidemic progress that kills the upper leaves of adult plants before grain filling. Pictures in this figure were captured in a wheat field after 3 years of monocropping. Photo credits by Leandro José Dallagnol.
Wheat seeds can be infected by Ptr during the grain-filling period, causing red smudge symptoms [38]. The fungus can survive on infected seed, contributing to the initial inoculum for the next season and facilitating the dispersal of the pathogen to new geographic areas [11, 31]. Seeds with red smudge negatively affect seedling emergence, seedling vigor, grain yield, and quality [11, 31].
2.3 Genetic variability
Ptr causes variable disease symptoms, and there are significant interactions among isolates, host genotypes, and environments [39]. The high genetic variability of Ptr can be explained by the homothallic or self-fertile nature (MAT1–1 and MAT1–2) of sexual reproduction that occurs on wheat stubble between crop seasons [40, 41, 42]. Although molecular studies of isolates from different regions have demonstrated high levels of polymorphisms, no correlation between geographic origin and pathogenicity or toxin production was clearly established [39, 43, 44]. A study using 12 microsatellite loci to characterize Ptr populations from Asia, Australia, Europe, North America, and South America showed a high level of genetic diversity and moderate to high population differentiation among continents [42]. The major source of incursions for other populations was from the European population, indicating that the pathogen can be transported to other geographic regions though infected seeds [42]. Conidia dispersed by wind and the long-distance movement of infected seeds may contribute to genetic variability independent of geographic origin of the isolate. Thus, knowledge of the genetic variability of Ptr is useful in the development of resistant cultivars; and the variability may be detected through race classification of the pathogen population.
In wheat, Ptr conidia germinate after contact with the host surface, and within 24 hours under high relative humidity, the fungus penetrates the host tissue [45]. Conidial germination is possible over a temperature range from 10 to 28°C. Germinating conidia form one to six germ tubes, although two to four is the most common, from basal (polar) and intercalary cells [46, 47]. Appressoria formation on the germ tubes is observed above the junction or in the anticlinal and periclinal walls of epidermal cells, occasionally on trichomes or over the stomatal complex independent of the level of host susceptibility [46, 48]. Appressorium formation normally begins within 3 to 6 hours after inoculation, but the speed of its formation may differ among the isolates of Ptr [49]. After an appressorium is formed, the infection peg develops over the anticlinal cell wall, and penetration occurs through the periclinal wall to enter the leaf directly or through stomata [46]. Several researchers have shown that penetration of epidermal wheat leaf cells by Ptr can occur through the stomatal complex, the narrow epidermal cells running parallel to the leaf veins, or through trichomes [46, 47, 50, 51].
Appressorium formation is not a guarantee of infection. Sometimes, at the initial infection peg, under an appressorium occurs the formation of papilla or haloes, mainly in resistant hosts [52]. Nevertheless, the pathogen counteracts this defense mechanism by forming several appressoria on the same germ tube, increasing the probability of infection [13, 46, 47]. Thus, symptom expression may occur in the wheat plant regardless of the susceptibility or resistance of the cultivar. In resistant genotypes, fungal invasion of the mesophyll is restricted, causing the formation of only a few small spots or lesions on the leaves. On the other hand, in susceptible cultivars, the hyphae grow continuously through the mesophyll cells and develop into visible lesions [11, 46, 47].
Ptr induces tan-colored, necrotic lesions that are often surrounded by chlorotic borders or haloes with a small black point in the center, especially on susceptible wheat genotypes (Figure 2). When disease is severe, the lesions may coalesce, turning the leaves yellow, which senesce and die (Figures 2 and 3) [11]. In contrast, on resistant or moderately resistant genotypes, lesion size is reduced, and there is a lack of chlorotic and/or necrotic symptoms, despite the production of toxins [36, 53].
Figure 3.
Defense responses of susceptible (Fundacep Horizonte) and moderately resistant (Quartzo) wheat cultivars during the first 144 hours after contact with Pyrenophora tritiici-repentis race 1. The most evident differences between cultivars were the early and long activation of the defense response by H2O2 accumulation, epidermal cell fluorescence, enzyme activity (especially chitinase and lipoxygenase), and the diversity of phenylpropanoid derivatives in Quartzo, resulting in fewer and smaller lesions, as well as a thin halo around the lesions compared with Fundacep Horizonte. H2O2: hydrogen peroxide; CAT: catalase; POX: peroxidase; SOD: superoxide dismutase; CHI: chitinase; LOX; lipoxygenase; TSP: total soluble phenols; fluorescent cells: fluorescence analysis of the penetration sites of P. tritici-repentis on epidermal cells using a fluorescence microscope coupled with BP460–490 filters for visualization of fluorescent compounds such as phenolics; CA: caffeic acid; FA: ferulic acid; HA: hydroxybenzoic acid; SA: syringic acid, Hes: hesperetin, Kae: kaempferol; Lut: luteolin; Rut: rutin. Design figure credit by Leandro José Dallagnol.
3.2 Wheat defense mechanism
Wheat defenses against tan spot involve various mechanisms that are orchestrated during pathogenesis. Research on the wheat-Ptr interaction has shown how the activation of the defense response and its timeline vary between a susceptible and a moderately resistant cultivar [35]. In a moderately resistant cultivar, there was a more rapid response to the pathogen and a greater accumulation of hydrogen peroxide (H2O2) in the epidermal cells than in a susceptible cultivar (Figure 3). The accumulation of H2O2 is known to be a mechanism of the pathogen attack inducing cell death through Ptr toxins [26]. However, the early (<12 hours after inoculation) accumulation of H2O2 in the epidermal cell of the moderately resistant cultivar, compared to late accumulation (>24 after inoculation) in the mesophyll and epidermal cells of the susceptible cultivar, indicated that H2O2 was a defense mechanism in the moderately resistant cultivar. This is because the accumulation occurred before pathogen penetration into the leaf tissue and was related to lower infection efficiency (the ratio between the number of conidia on the leaf surface and the number of lesions formed). In the same moderately resistant cultivar, early fluorescence in epidermal cells, in neighboring cells, and in the cells that Ptr attempted to penetrate indicated phenylpropanoid derivative accumulation [54]. Some of these compounds showed fungitoxic effects including fungal hyphal tip swelling, granulation of germ tubes and hyphae, and hyphal hyperbranching, as well as the inhibition of conidial germination [54]. In addition, the activation of lipoxygenase and an early increase in the activity of the chitinases were observed to be greater in a moderately resistant cultivar compared with a susceptible cultivar [35]. Together, these studies provide important insights into the early, intense, and more diversified defense response activated in moderately resistant cultivars, resulting in an increased incubation period and a reduction in the number and size of lesions and thus reduced tan spot severity [19, 35].
3.3 Genetic wheat-Ptr interaction
Ptr infects all types of wheat including tetraploid (Triticum ssp. durum (Desf.) Husnot., 2n = 4x = 28, AABB genomes) and hexaploid (T. aestivum L., 2n = 6x = 42, AABBDD genomes) and their relatives [15]. The wheat–Ptr pathosystem involves multiple interactions between necrotrophic effectors (NEs) secreted by Ptr and host sensitivity genes [3]. The Ptr NEs are recognized by, at least, three independent corresponding genes in the host [55]; thus, diseases caused by necrotrophic pathogens such as Ptr are complex; they follow the inverse of the classical gene-for-gene model [56]. In the case of tan spot, a compatible interaction occurs when NEs produced by the pathogen meets the target in the host, which is the product of the corresponding host sensitivity gene, activating a signaling cascade that leads to host susceptibility [57, 58]. Therefore, susceptibility is dominant, and resistance is due to the lack of NE-host receptor interactions. Thus, the lack of host receptors results in the absence of the binding target for NEs, so the signaling cascade is not activated, resulting in an incompatible interaction [57]. Likewise, if the pathogen does not produce the NEs to the corresponding sensitive gene of the host, the result is a resistant response (Table 1).
Pyrenophora tritici-repentis susceptibility/sensitivity, recessive resistance, and major dominant resistance genes.
Three NEs (two proteinaceous and one non-proteinaceous, which are also considered as host-specific toxins) were identified in Ptr [76]. The first NE to be identified, isolated, and characterized was ToxA, a 13.2 kDa protein encoded by the ToxA gene, which causes necrotic symptoms [77]; it is considered as a major virulence component of wheat pathogens on the Tsn1 gene [78]. The ToxA gene seems to have been a horizontal transfer among genomes of three wheat pathogens, Ptr, Parastagonospora nodorum (=Stagonospora nodorum), and Bipolaris sorokiniana [79, 80, 81]. The mode of action of Ptr ToxA may be associated with the arginyl-glycyl-aspartyl (RGD) motif, which plays a role in the interaction with integrin proteins and results in necrosis on sensitive cultivars [82, 83, 84].
The role of the Tsn1-Ptr ToxA interaction in tan spot susceptibility was evaluated in a tetraploid wheat and subspecies [26]. However, Tsn1-ToxA interaction was not associated with the development of tan spot [67, 85, 86, 87]. The Tsn1 gene in wheat is considered as R gene [88]; its structure encodes protein kinases, nucleotide binding site, leucine-rich repeat (NBS-LRR) domains, serine/threonine protein kinase (S/TPK) domains, and members of the wall-associated kinase class of receptors [89]. Thus, studies involving the Tsn1-Ptr ToxA interaction have indicated that NE sensitivity does not always define tan spot susceptibility; the Tsn1-PtrToxA interaction in disease development depends on the genetic background of the host [16, 80, 86, 90, 91, 92, 93]. In addition, the presence of ToxA and Tsn1 enhances disease symptoms, and in the absence of the Tsn1 gene, wheat is less susceptible to the most common pathogen races [43]. For instance, it has been suggested that the removal of the Tsn1 genes could minimize the damage caused not only by tan spot but also by Septoria nodorum blotch [67, 94].
Another NE is Ptr ToxB, a 6.5 kD protein encoded by the multicopy ToxB gene. It is much more variable in sequence among isolates than Ptr ToxA [95, 96] and causes chlorotic lesions on sensitive wheat cultivars [26]. Less is known about the mode of action of Ptr ToxB compared to Ptr ToxA; however, it was reported to decrease chlorophyll a (Chla) and b (Chlb) production, inducing chlorosis. Although the mode of action is not well understood, it has been shown that chlorosis is light-dependent and might involve the production of reactive oxygen species (ROS) [97]. This toxin is found not only in Ptr; it also has been described in other Pyrenophora species such as Pyrenophora bromi (Died.) Drechsler, which produces a homologous ToxB [98]. The ToxA and ToxB activate host resistance responses, similar to that in plant resistance to biotrophic pathogens. Those toxins produce responses in host plants related with gene regulation, resistant response, and photosynthesis changes [84, 99, 100, 101]. A recent study has showed the involvement of large mobile elements associated with Ptr’s effectors for ToxA and ToxB contributing to the highly plastic nature of the Ptr genome, which has helped to drive its worldwide adaptation [102].
The sensitivity gene Tsc2 (=Tsr6) interacts with Ptr ToxB, and this interaction plays a prominent role in the development of tan spot in tetraploid wheat [62, 95]. However, less is known of this interaction compared to Tsn1-PtrToxA, and some hexaploid wheat and Chinese Spring cultivars have been shown to be insensitive to ToxB [103, 104]. Marker development has facilitated the identification of sensitivity to ToxB in wheat [105].
The third toxin, Ptr ToxC, has been only partially characterized. It appears to be a nonionic, polar, low-molecular-weight compound that causes chlorosis but on different wheat cultivars than Ptr ToxB. The Ptr ToxC insensitivity gene was designated tsc1 [55]. Ptr ToxC cannot be easily obtained and purified; therefore, the role of the Ptr ToxC-Tsc1 interaction in tan spot has not been extensively investigated, although QTL mapping studies have suggested the importance of its role [91, 92]. The Ptr ToxC-Tsc1 interaction is also important for disease in winter wheat, and the interaction was found to be variable depending on the pathogen race or isolate used. Kariyawasam et al. [91, 106] and Liu et al. [92] demonstrated that the Ptr ToxA-Tsn1 and Ptr ToxC-Tsc1 interactions had additive contributions to disease severity in a spring wheat population. In addition to the three previously reported NEs, a putative Ptr ToxD was reported from culture filtrates of isolates that elicited chlorosis [83] or induced necrosis [107] on specific wheat genotypes; however, Ptr ToxD has not been described since.
3.4 Ptr race classification system and its distribution worldwide
Races of Ptr are determined by the number of toxins ((Ptr ToxA, Ptr ToxB, or Ptr ToxC) that interact directly or indirectly with the products of dominant host genes ((Tsn1 (=Tsr1), Tsc2 (=Tsr6), and Tsc1), leading to chlorotic and/or necrotic symptoms on the differential series. Currently, the characterization of Ptr races is performed on seven wheat lines/cultivars, including Glenlea, Katepwa, 6B662, 6B365, Salamouni, Coulter, and 4B1149 [3, 53, 108, 109]. Eight races (Table 2) are recognized according to the symptoms caused on the differential genotypes [108].
Tox
Necrosis
Chlorosis
No symptoms
Race 1
Ptr ToxA Ptr ToxC
Glenlea, Katepwa, and Coulter
6B365
Salamouni and 4B1149
Race 2
Ptr ToxA
Glenlea, Katepwa, and Coulter
—
Salamouni and 4B1149
Race 3
Ptr ToxC
Coulter
6B365
Salamouni and 4B1149
Race 4
None/avirulent
Coulter
—
Salamouni and 4B1149
Race 5
Ptr ToxB
Coulter
Katepwa and 6B662
Salamouni and 4B1149
Race 6
Ptr ToxB Ptr ToxC
Coulter
Katepwa and 6B662, 6B365
Salamouni and 4B1149
Race 7
Ptr ToxA Ptr ToxB
Glenlea, Katepwa, and Coulter
Katepwa and 6B662
Salamouni and 4B1149
Race 8
Ptr ToxA Ptr ToxB Ptr ToxC
Glenlea, Katepwa, and Coulter
Katepwa, 6B662 and 6B365
Salamouni and 4B1149
Table 2.
Races of Pyrenophora tritici-repentis classified according to symptoms (necrosis and or chlorosis) or lack of symptoms produced on differential wheat genotypes (Glenlea, Katepwa, 6B365, 6B662, Coulter, 4B1149, and Salamouni) due to toxins PtrToxA, PtrToxB, and Ptr ToxC.
The races of Ptr have been reported worldwide, but their prevalence varies among locations. Races 1 and 2 are the most common because the majority of isolates produce ToxA, and half of the Ptr populations produce ToxC [110]. Several studies reported races 1 and 2 to be predominant in Australia, Argentina, Brazil, Canada, Kazakhstan, and the United States [9, 39, 77, 111, 112, 113, 114]. Isolates containing ToxA are genetically similar to each other and different from those lacking this toxin [40].
Races 3, 4, and 5 are less frequent than races 1 and 2, and they occur mainly in North American, the Caucasus, and some European countries; outside these regions, only race 4 has been reported in Argentina (Table 3).
Races of Pyrenophora tritici-repentis reported worldwide.
Worldwide, the avirulent race 4 has been observed less frequently than other races [126]. Race 5 is mainly found in North Africa, although it has also been found in the Ptr population from Canada, the United States, Syria, Azerbaijan, and Germany but less frequently compared to races 1, 2, or 3 [96, 109, 112, 118]. The ToxB isolates are highly conserved among a geographically diverse set of isolates [131]. In the Canadian population, the ToxB isolates are few and less virulent compared to the Algerian population [96, 110]. Nevertheless, the ToxB isolates are a threat in Canada as nearly all Canadian wheat cultivars are susceptible to this toxin [9, 132].
The presence of races 6, 7, and 8 was reported in populations from North Africa, the Caucasus, and the Middle East. Race 6 of Ptr has been found mainly in Algeria and Morocco [96], while races 7 and 8 have been reported from Azerbaijan, Syria, Turkey, and Russia and less frequently from North Africa [109, 110, 133, 134]. These races are not reported in North America, and only race 8 was once reported in South America [109]. Races 6, 7, and 8 are mainly found in the Middle East and the Caucasus, but they are less common than races 1 and 2.
Variability of Ptr is observed in all populations evaluated worldwide, although separation of races by geographic region at the molecular level is inconclusive. Accurate race classification based on the current set of differentials should include both phenotypic and genotypic characterization to reflect the close association between race identity and NEs production [111, 135]. In addition, the variation of Ptr-wheat interactions suggested the existence of a new homologous gene and the existence of additional host–NE interactions [16, 91, 93, 136, 137]. Reports on unclassified races were verified with a different virulence phenotype [29, 114]. For example, an atypical isolate from Arkansas evaluated in several wheat trials indicated that symptoms varied [138], suggesting the existence of new NEs that interact with an unidentified wheat sensitivity gene and the probable existence of new Ptr races [16, 67, 91, 106]. Furthermore, Benslimane et al. [127] added three tetraploid wheat genotypes to the differential set observing that some isolates produce necrosis only in tetraploid wheat genotypes, whereas the hexaploid wheat genotypes were resistant, identifying a new virulence pattern. Later, Benslimane et al. [136] reported the presence of the ToxA and ToxB genes in all isolates without any difference in those functional genes, even though the absence of symptoms on hexaploid and tetraploid wheat was observed, suggesting the existence of an unknown virulence type. Thus, deeper studies are needed that will undoubtedly lead to the discovery of new NEs produced by Ptr, which may improve our understanding of this complex pathossysten.
In past decades, concern for tan spot management has resulted in increased efforts to improve breeding for resistance through advances in wheat genetics and genomics. The use of genetic control is an economically and environmentally friendly practice. In this context the introduction of tan spot-resistant germplasm has been studied and cultivars with improved resistance developed.
Selection efficiency is improved by the identification of susceptibility/sensitivity genes and quantitative trait locus (QTL) for economically important traits and the development of associated molecular markers [60, 62, 73]. Currently, over 100 QTL associated with tan spot resistance have been discovered through mapping in both hexaploid and tetraploid wheats [16].
In addition, several genome-wide association studies have revealed numerous regions associated with resistance to tan spot [69, 128, 139]. Molecular markers are available for variants of the wheat sensitivity genes Tsc1-Ptr ToxA and Tsn1-Ptr ToxC [92, 140]; as result, it is expected that insensitive Tsn-1 alleles provide resistance to pathogens carrying ToxA, although other factors also influence leaf spot resistance [140]. Recently, crossing between a moderately resistant synthetic hexaploid wheat, TA4161-L1, and a susceptible winter wheat cultivar has allowed the identification of QTL that confers resistance to race 1 [141], and in three tetraploid wheat mapping populations, 12 QTL were identified that conferred resistance to race 2 [16]. However, more studies are needed to understand the function of those QTL on the genetic interactions between Ptr and wheat.
Additionally, it has been proposed that tan spot-resistant cultivars can be developed through the elimination of NE sensitivity genes from breeding material [67]. This will reduce the chances that the pathogen will evolve to become virulent on the host since the NE genes are not present. In a recent report, it was shown that both Ptr ToxA-Tsn1 and Ptr ToxC-Tsc1 interactions are important for tan spot development in winter wheat. The absence of these two Ptr sensitivity genes in wheat results in lines highly resistant to the pathogen [91], and new sources of numerous tetraploids and hexaploid wheat accessions lacking all three NEs are available. Several studies have identified a few recessive resistance genes against specific races or isolates of Ptr from hexaploid or tetraploid wheat accessions, including tsr2, tsr3, tsr4, and tsr5 [57, 62, 142].
Marker-assisted selection (MAS) is a useful way to pyramiding resistance genes or QTL to improve resistance to tan spot in breeding programs. Several tan spot resistance QTL were discovered using spring wheat landraces from both the USDA-ARS National Small Grains and the CIMMYT historical bread wheat collections [143, 144, 145]. In the 2017–2018 crop season, Kokhmetova et al. [104] conducted screening and molecular marker analysis of wheat germplasm and selected 27 wheat accessions insensitive to ToxA. The accessions expressed a resistant reaction to Ptr when inoculated with spores of race 1, as well as field resistance to the pathogen. Recently, a single dominant gene (designed Tsr7) found in tetraploid and hexaploid wheats has been reported to condition race-nonspecific resistance to Ptr [15]. Mapping showed that the Tsr7 locus is likely in the same previously identified QTL in the hexaploid wheat cultivars BR34 and Penawawa that provide race-nonspecific resistance. The authors also reported that four SNP-based semi-thermal asymmetric reverse PCR (STARP) markers cosegregated with Tsr7. These findings provide useful insight for the use of MAS to select for tan spot resistance.
Sources of tan spot resistance can be found in collections of wheat germplasm from around the world including Aegilops tauschii accessions [146, 147] tetraploid wheat relatives [86], wheat–alien species derivatives [148], synthetic hexaploid wheat lines [149, 150], spring wheat landraces from the USDA-ARS National Small Grains collection, the CIMMYT historical bread wheat collection [143, 144], the European winter wheat collection [139], North American winter wheat cultivars and breeding lines [94], and the Vavilov wheat collection [37, 128, 151].
The largest and most diverse wheat collection in the world is housed at the N. I. Vavilov Institute of Plant Genetic Resources in St. Petersburg, Russia, where there are 38,000 cataloged tetrapliod, hexaploid, and wild wheat accessions. Among this diverse collection of germplasm, materials were detected with resistance against leaf rust and Septoria leaf blotch, which can benefit wheat breeding. It is also an excellent source of genetic diversity for resistance to other wheat diseases [37, 128, 151, 152]. Wheat accessions from the Vavilov collection carrying adult-plant resistance (APR) and associated QTL displayed enhanced levels of resistance to Puccinia triticina, highlighting the potential for QTL stacking through breeding [37]. Interestedly, Dinglasan et al. [128] found a novel APR-QTL effective even in the presence of the host sensitivity gene Tsn1. These genomic regions could offer broad-spectrum tan spot protection not just to ToxA but also to other virulence factors. Consequently, APR could be used to improve resistance levels in modern wheat cultivars and contribute to the sustainable control of tan spot [128, 153].
Association mapping of 170 lines of historical hexaploid wheat germplasm developed at CIMMYT by Singh et al. [145] identified significant marker associations on chromosome arms with genotypic data generated by 1644 molecular markers. They reported two QTL, one on chromosome arm 6AL and the other on 7BL, to be novel regions for tan spot resistance. Kariyawasam et al. [106] identified a major race-nonspecific QTL on chromosome arm 3BL in a recombinant inbred wheat population derived from the cross between hexaploid wheat cultivars ‘Louise’ and ‘Penawawa’. An attempt was made to decipher the genetics and map resistance to Ptr and P. nodorum in the PBW343/Kenya Nyangumi (KN) population, which was comprised of 204 F6 recombinant inbred lines (RILs). The Ptr QTL on chromosome 1B was pleiotropic with the APR genes Lr46/Yr29/Pm39, which contribute to tan spot resistance [154]. In addition, Stadlmeier et al. [155] showed that a specific genetic region on chromosome 7AL has contrasting effects on resistance not only for tan spot but also for powdery mildew and Septoria tritici blotch.
The studies presented provide evidence that race-nonspecific resistance QTL plays an important role in governing the reaction of wheat to tan spot and that the disease is much more complex than the current race classification system suggests [91, 156].
In Brazil, there are commercial wheat cultivars that exhibit resistance to a wide range of diseases [157]. Brazilian breeders have developed and released several wheat cultivars that are moderately resistant to tan spot. Of 37 Brazilian wheat cultivars evaluated, 26 (70%) were insensitive to Ptr ToxA and Ptr ToxB, and 20 (55%) were assessed as resistant according to Lamari and Bernier [3], indicating that Brazilian genotypes are a good source of resistance to tan spot [111]. Brazilian cultivar selection follows a traditional method via natural infection through field trials [6], similar to the breeding programs in Argentina where there are only a few moderate resistance cultivars [158]. Therefore, in South America, tan spot-resistant cultivars are not the only strategy to manage the disease, and resistance should be used with other strategies implemented in an integrated disease management plan.
4.2 Chemical control
Chemical control is one of the strategies used to manage Ptr. The use of fungicides provides benefits but increases production costs [159]. Effective groups of fungicides to control tan spot include the triazoles, strobilurins, and carboxamides [12, 160, 161, 162].
Ptr is considered as a medium risk for the development of resistance to fungicides, but insensitivity to some fungicides on populations of Ptr has been reported. Isolates of Ptr with mutations such as G137R and F129L confer partial resistance, and G143A confers high levels of insensitivity to QoI fungicides [163, 164]. Sierotzki et al. [164] detected isolates of Ptr carrying mutations on the mitochondrial cytochrome b gene (CYTB) from Sweden, Germany, and Denmark. Recently, the G143A mutation, conferring QoI resistance, has been found in the Ptr population of Argentina [165]. Due to concerns with fungicide insensitivity, strobilurins are often mixed with other groups of fungicides, and they should be rotated with fungicides with other modes of action when used as a single active ingredient [166]. Other fungicides such as triazoles and carboximides are considered only medium risk, but cross-class resistance has been reported [129]. Therefore, attention to fungicide management must be taken in the control of Ptr, because once the pathogen has adapted to either DMI or QoI fungicides, the pathogen may become cross-resistant. General principles to reduce the risk of pathogen insensitivity to fungicides have been proposed by the Fungicide Resistance Action Committee [167]. These tactics need to be tested for specific fungicide-pathogen-crop combinations for each region or in different agrosystems.
The optimum timing of fungicide application depends on the severity of the disease, growth stage, and susceptibility of the host [168]. Some studies reported that the best application time for the control of leaf spots is at the flag leaf stage and Zadoks growth stage (ZGS) 39 and for the control of tan spot Stagonospora nodorum blotch, Septoria leaf blotch [169], and, specifically, spot blotch [170] in hard red spring wheat. On the other hand, it was proposed that one fungicide application during anthesis (ZGS60), which provides Fusarium head blight suppression, also provided adequate leaf spot disease control in western Canada [113].
To obtain the greatest benefit from fungicide application, growers must consider the previous crop history (previous crops in the rotation, previous occurrence of tan spot and its severity), the tan spot susceptibility of the cultivars grown, and the climatic conditions of the season (rainfall and temperature). In southern Brazil, tan spot occurs at the highest severity at the beginning of the season (during tillering or before), when susceptible cultivars are monocropped (wheat grown on wheat stubble). The first application of fungicide occurs at the stem elongation growth stage or earlier, followed by two or three more applications but respecting the requirements of the pre-harvest intervals (Dallagnol, L. J.; personal communication). Consequently, in environments favorable for tan spot, the selection of a cultivar with moderate resistance to tan spot and an effective fungicide, usually containing a premix of active ingredients of different chemical groups, along with the appropriate time of application, is important in an integrated leaf spot disease management program.
4.3 Cultural control
Some practices, such as soil tillage and crop rotation, significantly decrease the development of tan spot [171]. In the past decades, tan spot has increased in severity with the adoption of minimum and no-till seeding [8, 172]. Nevertheless, the impact of these practices on tan spot varies around the world. In some cases, no-till wheat production increases the amount of straw on the soil surface and slightly increases the severity of tan spot compared with conventional tillage [173, 174, 175]. For example, Jorgensen and Olsen [163] reported an increase in tan spot severity with reduced tillage compared to conventional tillage.
Other studies have indicated that over at least 4 years, leaf spot diseases were not greatly affected by soil tillage systems [13]. Furthermore, in a survey of commercial wheat crops there was little effect of agronomic practice on leaf spot severity, although there was increased isolation of Ptr from fields under no-till management compared with conventional tillage [176]. Environmental factors are often more important than the tillage system for disease development [177]. Under both conventional and no-till, leaf disease development may be more severe in favorable disease years, but in years when the climate is not favorable for disease, differences in tillage system were not observed [178, 179].
Crop rotation is an important strategy to reduce the risk of leaf spot diseases. Numerous studies have shown that growing a crop on its own stubble usually leads to greater disease severity for residue-borne diseases compared with production on crop stubbles of different species [175, 180, 181, 182, 183]. For Ptr, which survives as pseudothecia and mycelium on wheat debris, wheat seedlings developing near contaminated debris may be exposed to high concentrations of inoculum during the growing season, compromising plant development and increasing the risk of secondary inoculum and epidemic development (Figure 2). Tan spot in particular was reported to be lower when spring wheat was grown on the stubble of crops other than wheat, for example, after barley (H. vulgare), canola (Brassica napus L.), crambe (Crambe abyssinica H.), sorghum (Sorghum bicolor), flax (Linum usitatissimum), and lentil (Lensculinaris medikus) [181, 184, 185, 186]. Therefore, further studies are necessary on tan spot severity and wheat yield associated with the influence of previous crops (other than those cited above), crop residues, and time of residue decay to determine the best crop sequences.
4.4 Pathogen-free seed
Infected seed plays an important role in the epidemiology of tan spot. However, pathogen transmission from seed to seedling can be affected by many factors, such as the cultivar’s susceptibility, percentage seed infection, aggressiveness of the isolate, soil moisture, temperature, cropping practices, sowing depth, rainfall, and light [31]. Therefore, infected seed is still a source of inoculum, and seed testing for pathogens is advisable to properly distinguish among Pyrenophora species and determine the Ptr incidence [87, 111]. Seed-borne Ptr can be mitigated by seed-applied fungicide. Carmona et al. [187] reported that iprodione was effective on seed-borne fungal pathogens.
4.5 Fertilizer management
Wheat growing under optimal nutrition is less prone to disease development, but at least two elements confer remarkable effect on tan spot: nitrogen (N) and silicon (Si). These two elements have been studied for their impact on the disease in recent decades [20, 176, 179, 188, 189, 190].
An increase in the amount of N fertilizer applied and the proportion of N utilized in the form of ammonium were shown to reduce development of tan spot [189]; however, Bockus and Davis [188] suggested that the apparent reduction of disease from N fertilizer is due to a delay in leaf senescence rather than a direct effect on tan spot. Fleitas et al. [18] and Castro et al. [17] found that the combination of high N fertilization and fungicide application increased the quality of wheat produced and reduced tan spot severity. Supporting those results, experiments conducted in Brazil during 2019 and 2020 determined that increasing the N rate from 70 to 130 kg N ha−1, the use of a moderately resistant cultivar, and proper fungicide application reduce the severity of tan spot and increase wheat yield and nitrogen-use efficiency [191]. Therefore, N should be used appropriately, with the appropriate rate determined for each region.
With regard to Si, calcium silicate fertilizer is a source of soluble Si; it may be a potential strategy against tan spot. Experiments in the laboratory, greenhouse, and field provided insights into the wheat defense mechanism against Ptr affected by Si, such as the resistance components affected, which was reflected in a reduction in the severity of tan spot in both the greenhouse and field. Laboratory studies showed that when Si was applied to a moderately resistant wheat cultivar, it enhanced the resistance to tan spot by increasing biochemical defense mechanisms and histo-cytological defense responses [35, 54]. The most important defense responses potentiated by Si included the early and more intense accumulation of hydrogen peroxide in the epidermal cells as well as phenylpropanoid derivatives at the infection site and the alteration of enzyme activities such as superoxide dismutase, catalase, peroxidase, quitinase, and phenylalanine ammonia lyase [35, 54]. Together, these defense responses restricted the spread of the pathogen and the damage caused in the plant tissues, resulting in a reduction in cell death at Ptr infection sites [54]. The defense responses affected by Si were associated with alterations in the resistance components of tan spot such as longer incubation period (time between plant inoculation and disease symptom appearance) and reduction of the relative infection efficiency, rate of lesion expansion (rate of spread of the pathogen/toxins in the plant tissue), lesion size (leaf area affected by individual lesion), and disease severity (percentage of total foliar area of the plant affected by the disease) [36, 54].
In the field, fertilization with calcium silicate reduced tan spot severity up to 50% and increased grain yield by 1 tonne per hectare [19]. Furthermore, wheat plants grown in soil fertilized with calcium silicate that received one application of fungicide at the stem elongation growth stage had tan spot severity and grain yield similar to plants grown in soil fertilized with limestone and treated twice with fungicide (stem elongation and flowering stages). Thus, the effects of Si depend on the absorption capacity of the cultivar and the availability of the element in the soil; it may be an additional strategy for the integrated management of tan spot.
4.6 Biological control
Some biocontrol agents have been tested for the control of Ptr to minimize the use of fungicides. Results under laboratory and greenhouse conditions have indicated the potential of Trichoderma spp. for the control for Ptr [192], in particular T. hamatum [123]. Tan spot severity was reduced when T. harzianum and T. koningii were applied to wheat under field conditions [193]. Furthermore, other potential biological agents to control Ptr have been tested such as Myrothecium roridum, Acremoniun terricola, Stachybotrys sp. [193, 194], Laetisaria arvalis and Limonomyces roseipellis (inhibitory to pseudothecia development) [185, 195], Chaetomium sp. [196], and Bacillus sp. [123]. However, more field research is needed to understand the potential of these biocontrol agents for the management of tan spot.
Implementing an effective, economic, and lasting tan spot management strategy is not a simple task; there are many factors and risks to consider. In past decades, knowledge of NEs and host genes have been used in breeding programs, but some evidence exists of new interactions between novel NEs and host genes that need to be characterized to understand their role in governing tan spot susceptibility [156]. For this reason, capturing the genomes of multiple races from diverse geographic regions will be important for the identification and isolation of novel effectors. In this way, molecular cloning of sensitive genes and broad-spectrum resistance genes will allow more suitable characterization of wheat–Ptr interactions and shed light on the relationship between qualitative and quantitative resistance mechanisms at the molecular level [16, 121].
For breeding purposes, the development of functional markers through genomic research will provide enhanced germplasm for resistance. Hence, effector-assisted selection, marked-assisted selection, and genome-wide association have been used for the identification of molecular markers linked with resistance or susceptibility [16, 60, 103, 128, 197]. These tools can be used to pyramid insensitivity genes or to remove some sensitivity genes from potential germplasm for effective long-term control of tan spot.
It will be important to continue to evaluate wild wheat relatives, alien species, and potential germplasm to identify new sources of resistance to tan spot [141]. Currently, material with resistance has been studied and some QTL associated with resistance identified; some materials have been proven to have a broad spectrum of resistance to multiple diseases. Therefore, their use can be an excellent source of genetic diversity in wheat disease management, especially tan spot under field conditions.
Integrated disease control strategies are important tools to manage tan spot. To achieve desirable results, multiple disease mitigation strategies should be incorporated into the management program such as the use of resistant genotypes, crop rotations, pathogen-free seed, fungicide seed treatment, appropriate fertilizer application, and judicious use of foliar fungicide applied based on predicted disease development and at the optimum time in a manner as environmentally friendly and cost-effective as possible.
Finally, a holistic view must be considered for efficient and sustainable management of tan spot including the use of pathogen-free seed, crop rotation, and other methods to reduce initial inoculum. The application of foliar fungicide is a complementary strategy when resistant cultivars are not available or the resistance not sufficient; identifying the correct application timing be determined according the region. Furthermore, attention to the influence of nutrition on the Ptr-wheat pathosystem must be considered because there is a potential benefit from N and Si fertilization. Both must be considered as alternative strategies following recommendations to reduce the damage of tan spot.
The authors are thankful to CAPES for financial support and the student scholarship (Finance code 001) to A. Román. L.J. Dallagnol is supported by fellowship (grant number 305247/2021-2) from Brazilian National Council for Scientific and Technological Development (CNPq).
The authors declare that they have no conflict of interest.
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Written By
Andrea Elizabeth Román Ramos, Hadley Randy Kutcher and Leandro José Dallagnol
Submitted: 20 December 2022Reviewed: 31 January 2023Published: 28 February 2023
Open access peer-reviewed chapter - ONLINE FIRST
