Septoria tritici and Septoria nodorum Biology

Following Erick De Wolf, Septoria Tritici Blotch, Kansas State University, April 2008 Septoria tritici blotch known as speckled leaf blotch, is caused by the fungus Septoria tritici. It is distributed in all wheat-growing areas of the world and is a serious problem in many regions. Septoria tritici blotch is most damaging when the disease attacks the upper leaves and heads of susceptible varieties late in the season.


Septoria tritici blotch symptoms first appear in the fall. The initial symptoms are small yellow spots on the leaves. These lesions often become light tan as they age, and the fungal fruiting bodies can be seen embedded in the lesions on the awns. Lesions are irregularly shaped and range from elliptical to long and narrow (Figure 1). Lesions contain small, round, black speckles that are the fruiting bodies of the fungus (Figure 2). The black fruiting bodies look like grains of black pepper and can usually be seen without the aid of a magnifying glass. The disease begins on the lower leaves and gradually progresses to the flag leaf. Leaf sheaths are also susceptible to attack. In wet years, the speckled leaf blotch fungus can move onto the heads and cause brown lesions on the glumes and awns known as glume blotch. These lesions often become light tan as they age and the fungal fruiting bodies are often seen embedded in the lesions on the awns.
The glume blotch phase can cause significant yield loss, but the relationship between disease severity and yield loss is not well understood. Septoria tritici blotch can be confused with other leaf diseases that have very similar symptoms: tan spot and Stagonspora nodorum blotch, for example. It is common for plants to be infected by more than one of these foliar diseases, and it may require laboratory examination to accurately diagnose which diseases are most prevalent. Laboratory examination is nearly always required to distinguish the cause of glume blotch. Knowing the species is not important for spray decisions because all three diseases respond similarly to fungicides. However, knowing which diseases are most prevalent is an important part of variety selection because different genes control the resistance to the diseases.
The most reliable way to distinguish Septoria tritici blotch from the other diseases is by the presence of the black fungal fruiting bodies. The fungus that causes tan spot does not produce this type of reproductive structure. However, under moist conditions, the fungus that causes Stagonospora nodorum blotch will produce light brown fruiting bodies. In addition to the color difference, these structures are also smaller than those produced by Septoria tritici.

Life Cycle

Septoria tritici survives through the summer on residues of a previous wheat crop and initiates infections in the fall. There is some evidence that the fungus is able to survive in association with other grass hosts and wheat seed. These sources of the fungus are probably most important when the wheat residues are absent. Regardless of rotation or residue management practices, there is usually enough inoculum to initiate fall infections. Septoria tritici blotch is favored by cool, wet weather. The optimum temperature range is 16 to 21 °C; however, infections can occur during the winter months at temperatures as low as 5°C. Infection requires at least 6 hours of leaf wetness, and up to 48 hours of wetness are required for maximum infection. Once infection has occurred, the fungus takes 21 to 28 days to develop the characteristic black fruiting bodies and produce a new generation of spores. The spores produced in these fruiting bodies are exuded in sticky masses and require rain to splash them onto the upper leaves and heads.

Infection by Septoria tritici: Pycnidiospores of S. tritici germinate in free water from both ends of the spore or from intercalary cells (Weber, 1922). Spore germination does not begin until about 12 hours after contact with the leaf. Germ tubes grow randomly over the leaf surface. Weber (1922) observed only direct penetration between epidermal cells, but others concluded that penetration through both open and closed stomata is the primary means of host penetration (Benedict, 1971; Cohen and Eyal, 1993; Hilu and Bever, 1957). Kema et al. (1996) observed only stomatal penetration. Hyphae growing through stomata become constricted to about 1 μm diameter, then become wider after reaching the substomatal cavity.
Hyphae grow parallel to the leaf surface under epidermal cells, then through the mesophyll to cells of lower the epidermis, but not into the epidermis. No haustoria are formed and hyphal growth is limited by sclerenchyma cells around the vascular bundles, except when hyphae are very dense. Vascular bundles are not invaded. Hyphae grow intercellularly along cell walls through the mesophyll, branching at a septum or middle of a cell. No macroscopic symptoms appear for about 9 days except for an occasional dead cell, but mesophyll cells die rapidly after 11 days. Pycnidia develop in substomatal chambers. Hyphae seldom grow into host cells (Hilu and Bever, 1957; Kema et al, 1996; Weber, 1922).
Successful infection only occurs after at least 20 hours of high humidity. Only a few brown flecks developed if leaves remained wet for 5-10 hours after spore deposition (Holmes and Colhoun, 1974) or up to 24 hours (Kema et al., 1996). Host-parasite relations are the same on resistant or susceptible wheats. Spore germination on the leaf surface is the same regardless of susceptibility. The number of successful penetrations is about the same, but hyphal growth is faster in susceptible cultivars, resulting in more lesions. Hyphae extend 44 Session 2 — B.M. Cunfer beyond the necrotic area in all cultivars. A toxin may play a role in pathogenesis (Cohen and Eyal, 1993; Hilu and Bever, 1957). In contrast, colonization was greatly reduced on a resistant line (Kema et al., 1996).

Stagonospora (Septoria) and Septoria Pathogens of Cereals: The Infection Process

B.M. Cunfer, Department of Plant Pathology, University of Georgia, Griffin, GA

The infection process has been studied most intensely for Stagonospora (Septoria) nodorum and Septoria tritici. One in-depth study on Septoria passerinii is available. Nearly all of the information reported is for infection by pycnidiospores. However, the infection process for other spore forms is quite similar. The information presented is mostly for infection of leaves under optimum conditions. Some studies were done with intact seedling plants, whereas others were conducted with detached leaves. Infection of the wheat coleoptile and seedling by S. nodorum was described in detail by Baker (1971) and reviewed by Cunfer (1983). Although no precise comparisons have been made, it appears that the infection process has many similarities in each host-parasite system and is typical of many necrotrophic pathogens. Information on factors influencing symptom development and disease expression are excluded but have been reviewed by other authors (Eyal et al., 1987; King et al., 1983; Shipton et al., 1971). A summary of factors affecting spore longevity on the leaf surface is included.

Role of the Cirrus and Spore Survival on the Leaf Surface The most detailed information on the function of the cirrus encasing the pycnidiospores exuded from the pycnidium is for S. nodorum. The cirrus is a gel composed of proteinatous and saccharide compounds. Its composition and function are similar to that of other fungi in the Sphaeropsidales (Fournet, 1969; Fournet et al., 1970; Griffiths and Peverett, 1980). The primary roles of cirrus components are protection of pycnidiospores from dessication and prevention of premature germination.
The cirrus protects the pycnidiospores so that some remain viable at least 28 days (Fournet, 1969). When the cirrus was diluted with water, if the concentration of cirrus solution was >20%, less that 10% of pycnidiospores germinated. At a lower concentration, the components provide nutrients that stimulate spore germination and elongation of germ tubes. Germ tube length increased up to 15% cirrus concentration, then declined moderately at higher concentrations (Harrower, 1976).  Brennan et al. (1986) reported greater germination in dilute cirrus fluid. Cirrus components reduced germination at 10-60% relative humidity. Once spores are dispersed, the stimulatory effects of the cirrus fluid are probably negligible (Griffiths and Peverett, 1980).
At 35-45% relative humidity, spores of S. tritici in cirri remained viable at least 60 days (Gough and Lee, 1985). The cirrus components may act as an inhibitor of spore germination, or the high osmotic potential of the cirrus may prevent germination. Pycnidiospores of S. nodorum did not survive for 24 hours at relative humidity above 80% at 20 C. Spores survived two weeks or more at <10% relative humidity (Griffiths and Peverett, 1980). When the cirrus fluid of S. nodorum was diluted with water, about twothirds of the pycnidiospores lost viability within 8 hours, and after 30 hours in daylight, only 5% germinated. When spores were stored in the dark, 40% remained viable after 30 hours (Brennan et al., 1986).
Dry conidia of S. nodorum, shaded and in direct sunlight, survived outdoors at least 56 hours (Fernandes and Hendrix, 1986a). Germination of S. nodorum pycnidiospores was inhibited by continuous UV-B (280-320 nm), whereas germination of S. tritici was not. Germ tube extension under continuous UV-B was inhibited for both fungi, compared with darkness (Rasanayagam et al., 1995).


Infection by Septoria nodorum

The process of host penetration and development of S. nodorum within the leaf was examined in detail by several investigators (Baker and Smith, 1978, Bird and Ride 1981, Karjalainen and Lounatmaa, 1986; Keon and Hargreaves, 1984; Straley, 1979; Weber, 1922). Pycnidiospores tend to lodge in the depressions between two epidermal cells, and many attempted leaf penetrations begin there. Spores germinate on the leaf surface in response to free moisture (Fernandes and Hendrix, 1986b). They begin to germinate 2-3 hours after deposition, and after 8 hours germination can reach 90%. Leaf penetration begins about 10 hours after spore deposition (Bird and Ride, 1981; Brönnimann et al., 1972; Holmes and Colhoun, 1974).
At the onset of germination, the germ tube is surrounded by an amorphous material that attaches to the leaf. Germ tubes growing from either end of a spore and from intercalary cells tend to grow along the depressions between cells and are often oriented along the long axis of the leaf (O’Reilly and Downes, 1986). Hyphae from spores not in depressions grow randomly with occasional branching (Straley, 1979). An appressorium forms with an infection peg that penetrates the cuticle and periclinal walls of epidermal cells directly into the cell lumen, resulting in rapid cell death.
Many penetrations first are subcuticular or lateral growth of a hypha occurs within the cell wall before growth into the cytoplasm (Bird and Ride, 1981; O’Reilly and Downes, 1986). Penetration through both open and closed stomata also occurs and may be faster than direct penetration (Harrower, 1976; Jenkins, 1978; O’Reilly and Downes, 1986; Straley, 1979). Germ tubes branch at stomata and junctions of epidermal cells. Penetration of a germ tube into a stomate may occur without formation of an appressorium. Penetration sometimes occurs through trichomes (Straley, 1979). Apparently, most penetration attempts fail, with dense papillae formed in the cells at the site of attempted penetration (Karjalainen and Lounatmaa, 1986; Bird and Ride, 1981).
After penetration, epidermal cells die quickly and become lignified, and the hyphae grow into the mesophyll. Mesophyll cells become misshapen, and lignified material is deposited outside of some cells, which then collapse. Lignification occurs before hyphae reach the cell. The process is the same in all cultivars but develops more slowly in resistant cultivars. The hyphae grow intercellularly among epidermal cells, then into the mesophyll. When the mesophyll is penetrated, chloroplast deterioration begins in 6-9 days (Karjalainen and Lounatmaa, 1986).
However, the photosynthetic rate begins to decline within a day after infection and before symptoms are visible (Krupinsky et al, 1973). Sclerenchyma tissue around vascular bundles prevents infection of vascular tissue. The vascular bundles block the spread of hyphae through the mesophyll except when sclerenchyma tissue is young and not fully formed (Baker and Smith, 1978).
Stagonospora nodorum releases a wide range of cell wall degrading enzymes including amylase, pectin methyl esterase, polygalacturonases, xylanases, and cellulase in vitro and during infection of wheat leaves (Baker, 1969; Lehtinen, 1993; Magro, 1984). The information related to cell wall degradation by enzymes agrees with histological observations.These enzymes may act in conjunction with toxins. Enzyme sensitivity may be related to resistance and rate of fungal colonization (Magro, 1984). Like many necrotrophs, Septoria and Stagonospora pathogens produce phytotoxic compounds in vitro. Cell deterioration and death in advance of hyphal growth into mesophyll tissue (Bird and Ride, 1981) is consistent with toxin production. However, a definitive role for toxins in the infection process and their relation to host resistance has not been established (Bethenod et al, 1982; Bousquet et al, 1980; Essad and Bousquet, 1981; King et al, 1983). Differences in host range between wheat and barleyadapted strains of S. nodorum may be related to toxin production (Bousquet and Kollmann, 1998). Initiation of spore germination and percentage of spores germinated are not influenced by host susceptibility (Bird and Ride, 1981; Morgan 1974; Straley, 1979; Straley and Scharen, 1979; Baker and Smith, 1978).
Bird and Ride (1981) reported that extension of germ tubes on the leaf surface was slower on resistant than on susceptible cultivars. This mechanism, expressed at least 48 hours after spore deposition, indicates pre-penetration resistance to elongation of germ tubes. There were fewer successful penetrations in resistant cultivars, and penetration proceeded more slowly on resistant cultivars (Baker and Smith, 1978; Bird and Ride, 1981). Lignification was proposed to limit infection in both resistant and susceptible cultivars, but other factors slowed fungal development in resistant lines. In susceptible lines, faster growing Hyphae may escape lignification of host cells.Four days after inoculation of barley with a wheat biotype isolate of S. nodorum, hyphae grew through the cuticle and sometimes in outer cellulose layers of epidermal cell walls. Thick papillae were deposited beneath the penetration hyphae and the cells were not penetrated (Keon and Hargreaves, 1984).

Infection by Septoria passerinii: Green and Dickson (1957) present a detailed description of the infection process of S. passerinii on barley. The infection process is similar to S. tritici. Like S. tritici, the length of time required for leaf penetration is considerably longer than for S. nodorum. Germ tubes branch and grow over the leaf surface at random, but sometimes along depressions between epidermal cells. Leaf penetration is almost exclusively through stomata. Germination hyphae become swollen, and if penetration is unsuccessful, hyphae  continue to elongate. No penetration occurs 48 hours after spore deposition. After 72 hours, germ tubes thicken over stomata, grow between guard cells and on urfaces of accessary cells and into the substomatal cavities. Direct penetration between epidermal cells is seen only rarely.
Spore germination and host penetration are the same on resistant and susceptible cultivars. There is much less extension of hyphae within leaves on resistant cultivars and papillae are observed on many but not all cell walls. Hyphae grow beneath the epidermis from one stoma to another, but do not penetrate between epidermal cells. The mesophyll is colonized, but no haustoria form. After the mesophyll cells become necrotic, epidermal cells collapse. Mycelial development in the leaf is sparse and usually blocked by vascular bundles. In younger leaves, if the vascular sheath is less developed, hyphae pass between the bundle and the epidermis. Pycnidia form in substomatal cavities, mostly on the upper leaf surface (Green and Dickson, 1957).

Factors Affecting Spore Longevity on the Leaf Surface Among the Stagonospora and Septoria pathogens of cereals, definitive information on the infection process has been reported only for S. nodorum, S. tritici, and S. passerinii. Like many other necrotrophic pathogens, neither group of pathogens elicit the hypersensitive reaction. A significant difference in the infection process between Septoria and Stagonospora pathogens is that spore germination and penetration proceeds much faster for S. nodorum than for S. tritici and S. passerinii. This has a significant influence on disease epidemiology.
The Septoria pathogens penetrate the plant primarily through stomata, whereas S. nodorum penetrates both directly and through stomata. S. nodorum penetrates and kills the epidermal cells quickly, but S. tritici and S. passerinii do not kill epidermal cells until hyphae have ramified through the leaf mesophyll and rapid necrosis begins. Histological studies of fungal growth following host penetration match the data generated from epidemiological studies of host resistance. Resistance slows the rate of host colonization but has no appreciable effect on the process of lesion development.
The mechanisms controlling host response, whether related to enzymes and toxins or other metabolites released by the pathogens during infection, are still unclear. There is little information about infection by ascospores. The infection process is probably very similar to that for pycnidiospores. Ascospores of Phaeosphaeria nodorum germinate over a wide range of temperatures, and their germ tubes penetrate the leaf directly. However, according to Rapilly et al. (1973), ascospores, unlike pycnidiospores, do not germinate in free water. Infection Cycles

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