José Antônio Martinelli
SUMMARY
Fodder oats are widely used in the world, particularly in subtropical and temperate zones. As a cereal, oat is subject to attack by many disease-causing micro-organisms, some of them causing severe damages. This article reviews most of the main oat diseases, with special emphasis on oats destined for fodder.
Oats are an important fodder and grain crop in countries of the southern cone of South America. Approximately 600 000 ha of oats are grown for grain in Argentina, Uruguay and southern Brazil, but more than 4 000 000 ha are grown for fodder (Matzembacher, 1999; Rebuffo, 1997; Trombetta, 1997), although in Brazil much of the fodder oat is Avena strigosa rather than A. sativa. In the subtropical to temperate climate of this region, oats are grown in the winter and used as a winter cover crop, as food for both livestock and humans, and as raw material for industrial use. It is the third most important winter crop in southern Brazil (Leonard and Martinelli, 2004).
As in South America, fodder oats are important in other large areas of the world, like Australia, North America and Europe, and in all these regions oat diseases are of major concern in crop management. Some diseases are caused by highly specialized, biotrophic pathogens, such as the rusts and powdery mildews, whose mechanisms of spread are very efficient, making some crop management, such as rotation, inefficient for their control. Other diseases are caused by less specialized pathogens, those called hemibiotrophic, whose biological life cycles differ considerably from the first group. For these, simple practices, such as seed dressing and crop rotation, can reduce the initial inoculum, so that the disease does not reach economic threshold levels. The viruses, especially Barley Yellow Dwarf Virus (BYDV), form a third group of pathogens, whose occurrence is associated with the pattern of distribution of their vectors, the aphids, which constitute another phytosanitary problem.
For evolutionary reasons, most of the pathogens that attack oats have a close relationship with the plant. So, in most areas where the environment suits the crop, it also favours the occurrence of the diseases that these pathogens cause. Some pathogens, however, are less adapted to the species or less robust in these environment, and they cause less serious, or sporadic, diseases.
Many diseases cause either serious direct damage, mainly by reduction of the fodder yield, or indirect damage, by compromising the quality of the product. Among those causing severe direct dam age are crown and stem rusts, leaf blotch caused by Pyrenophora spp. and Septoria spp., and BYDV. Other diseases, such as scab and ergot, can produce toxins in the grains and make them unsuitable for consumption by either animals or humans.
The aim of this chapter is to present the main diseases of fodder oats in the main production areas of the world. Emphasis is put on the characteristics of the diseases, their epidemiological aspects, their management and the commonest measures of control.
Figure 12.1
Pustules of Crown rust on oat leaves
caused by Puccinia coronata f.sp. avenae.
Crown rust is the most harmful disease that affects oats and it is distributed worldwide, having been observed in all areas where these crops are grown (Simons, 1985). Crown rust is one of the most important oat diseases in Brazil, Argentina and Uruguay. Grain yields are negatively correlated with crown rust severity (Chaves et al., 2002) and may be reduced by as much as 50 percent in susceptible cultivars (Martinelli, Federizzi and Benedetti, 1994). It is caused by Puccinia coronata f.sp. avenae (Figure 12.1), a heteroecious macrocyclic rust (Agrios, 1997).
One of the particularities of this disease is its capacity to attack several plant species. The uredial and telial phases occur on oats and other grasses, including all species of oats (Avena spp.), Secale cereale, Hordeum vulgare, Lolium spp., Festuca spp. and Bromus inermis, among others; the spermagonial and aecial phases occur on Rhamnus bushes, the alternate host (Browning, 1973; Harder and Haber, 1992).
Infection by the pathogen induces several structural, biochemical and physiological changes in its host. The more profound changes are brought about by intracellular invasion by the fungus and the formation of haustoria, but in the early stages of infection there are no direct physiological effects of the intercellular hyphae on the protoplasts of the host (Harder and Haber, 1992).
Alterations in photosynthesis occur during the development of the infection and, soon after the inoculation, a decrease in gaseous exchanges is observed in the whole leaf. The infected areas, initially discrete, expand with the progress of the infection and symptoms of the disease appear about five days after inoculation, characterized by yellow spots, associated with the presence of mycelium of the fungus within the tissues. At this stage, photosynthesis is slightly reduced in the infected areas, but not in those parts of the leaf without infection, where the process shows levels similar to healthy parts. During sporulation, typically eight days after inoculation, there is a reduction in the rate of photosynthesis throughout the whole leaf, although this reduction is more conspicuous in areas invaded by the fungus. Eleven days after inoculation, "green islands" are formed around those areas of the leaf associated with the mycelium of the fungus and photosynthesis is drastically inhibited in the whole leaf. In areas not infected by the mycelium of the pathogen, photosynthesis is very low, indicating that even in these areas the photosynthetic apparatus is seriously damaged. In the green islands of the leaves, photosynthesis is low, but detectable, indicating that some photosynthetic processes are still occurring (Scholes and Rolfe, 1996).
Disease symptoms appear as yellow pustules containing masses of urediospores, which are exposed after the rupture of the epidermis. These lesions are circular or oblong and occur in both surfaces of the foliar sheet and can reach other green parts of the plant, when the epidemic becomes more severe. After some weeks, the borders of the uredopustules can turn black, with teliospore formation. When the infected plants reach maturity, production of urediospores ceases and they are then replaced by teliospores (Browning, 1973; Simons, 1985; Harder and Haber, 1992).
Primary infections are caused by urediospores or aeciospores. In areas of subtropical and temperate climate, where oats are grown in winter, urediospores from volunteer plants that survive the summer are usually responsible for the primary infections of plants sown in autumn. In Europe and in North America, the alternate host, Rhamnus spp., is an important source of inoculum for the oats, since it contributes through sexual recombination to the great variability observed in the pathogen population. The teliospores on infected straw from the previous summer germinate in spring, producing basidiospores, which in turn infect young leaves of Rhamnus. These infections produce aecidia from which aeciospores arise and then infect the oats. In South America, teliospores of Puccinia coronata have no known survival function (Martinelli, 2000). The primary source of inoculum to infect oats in autumn comes from urediniospores produced on volunteer plants that survive the summer on the edges of fields of summer crops such as soybean, in fence lines and along roadsides. Prevailing wind patterns annually distribute urediniospores of Puccinia coronata in a cyclical pattern throughout the oat growing regions of Brazil, Argentina and Uruguay as a shared epidemiological system. Epidemics typically start early; sometimes while oats are still at the tillering stage. A. strigosa is less susceptible than A. sativa, but rust severities of 5-10 percent are common during the growing season (Leonard and Martinelli, 2004).
Urediospores and aeciospores of Puccinia coronata f.sp. avenae are spread by the wind and can travel long distances. Their germination needs free water on the leaf surface and infection occurs through the stomata. These two processes are favoured by temperatures between 10 and 25°C. Temperatures above 30°C inhibit the infection process (Simons, 1985).
The causal agent is Puccinia graminis Pers. f.sp. avenae Eriks. and Henn., which attacks all species of oats, including wild oats (Wallwork, 1992). Stem rust is a widespread disease of oats, occurring almost everywhere they are grown (Zillinsky, 1983). In Canada, it occurs almost every year in some provinces, including in Ontario, Quebec, Manitoba and eastern Saskatchewan, causing severe crop losses (Martens, Seaman and Atkinson, 1985). In Australia, it can be devastating, causing crop losses up to 100 percent (Wallwork, 1992). In South America, stem rust epidemics are typically at the end of the crop season, from booting stage onwards, when the temperature is warmer. In Argentina, where A. sativa is used as fodder, it is particularly serious because their cycle is longer than that in Brazil, where the importance of the disease has diminished because oats are harvested earlier (personal observation of the author).
Disease symptoms most commonly appear on the stems and leaf sheaths, but leaf blades and spikes may also become infected. Urediospores develop in pustules (uredia) that rupture the epidermis and expose masses of reddish-brown spores. The pustules are larger than those of crown rust, oval or elongated, with loose or torn epidermal tissue along their margins. They may appear on both surfaces of the leaf. They continue to be produced until the plants approach maturity. After that, teliospores develop, either in the same uredia or in other fruiting structures called telia.
Epidemics are more likely when weather is warm (15-30ºC) and conditions moist (Wallwork, 1992). Stem rust develops its sexual stage on Berberis vulgaris L. In North America, the disease is usually not as widespread as crown rust, probably because the alternate host is less common than Rhamnus cathartica (Harder and Haber, 1992). In the absence of the alternate host (South America and Australia) its distribution and epidemiology follows the same pattern as that of crown rust (Leonard and Martinelli, 2004).
Attempts to breed oat cultivars resistant to crown rust have been frustrated in most countries by the rapid appearance of new virulent races of Puccinia coronata, often within a few years of the release of cultivars, with new types of race-specific resistance. According to Federizzi and Stuthman (1998), the rapid breakdown of resistance observed in South America is due to the large population of P. coronata maintained in the uredinial stage throughout the year and the large numbers of mutations to virulence that occur annually in the pathogen population. Although a large number of genes for race-specific resistance to crown rust are available to oat breeders, information on occurrence of virulence to these genes in the South American populations of P. coronata has been largely lacking. Recently, efforts have been made to search for a more stable, quantitative, non-specific resistance to crown rust, such as the one provided by the A. sativa genotype MN841801 from the University of Minnesota breeding programme. In Brazil, Chaves, Martinelli and Frederizzi (2004a, b) were able to identify a number promising genotypes as sources of quantitative resistance.
There is a much more limited reservoir of resistance to stem rust, but known genes can provide effective and longterm resistance when used in appropriate combinations. In Argentina, the only oat variety currently in use that is resistant to stem rust is the genotype UFRGS-16, bred by the oat breeding programme of the Federal University of Rio Grande do Sul State.
Eradication of the alternate Rhamnus and Berberis hosts has been an important factor in reducing crown and stem rust epidemics in areas where these hosts play a major role as sources of inoculum and genetic variability for the pathogen. Berberis now plays a minor role in most of North America. Rhamnus is difficult to control and extensive infestations still remain, particularly in Ontario, Canada (Harder and Haber, 1992).
Escape is another important factor in reducing damage by the rusts. This can be achieved by advancing the planting dates or by using early maturing cultivars. Typically, no chemical control is used for crown or stem rusts on oats destined for pasture.
The causal agent of leaf blotch and darkening on oat grains is the fungus Pyrenophora chaetomioides Speg. Briosi and Cavara, cited by Dennis (1935), who made the first report of its imperfect stage, Drechslera avenae, in 1889, in the Pavia region of Italy. Initially it was named as Helminthosporium teres Sacc. form avenae-sativae. The name Pyrenophora chaetomioides Speg., the stage used for the description of the ascocarp, has precedence over the name Pyrenophora avenae Ito and Kurib. (1930), according to Sivanezan (1987).
Pyrenophora leaf blotch (Figure 12.2) has been reported from most areas of the world where oats are grown. In 1974, there were reports of epidemics of leaf blotch on oats in Germany and the south of the USA, where it appeared as the most severe disease after crown rust, with damage estimated at around 30-40 percent (Gough and McDaniel, 1974). It is also common as a seed-borne pathogen in Sweden and in Finland, where losses of up to 10 percent can occur; in India the disease has been reported as widespread from the seedling stage till plant maturity (Harder and Haber, 1992). In Brazil, P. chaetomioides is considered the main pathogen associated with oat seeds (Blum, 1997), although high severities of leaf spots are less common. So far, there is no evidence that this fungus produces toxins on either leaves or grains that could compromise the use of infected oats as fodder.
Figure 12.2
Symptoms of Leaf blotch and black
nodes on oat, caused by Pyrenophora chaetomioides
The most commonly observed symptoms of leaf blotch of oats appear on the leaves and, under favourable conditions for the disease, they can reach the sheaths and appear soon after their emergence (Ivanoff, 1963). Those symptoms were described by Ellis in 1971 as small spots initially (1-3 × 1-2 mm), with a white centre surrounded by a brown-reddish halo that later coalesce and expand, forming small longitudinal stripes. In conditions in the south of Brazil, the leaf blotches are prolonged longitudinally, with dark coloration, eventually becoming olive and with a greyish centre.
Another symptom, called blackstem or stem-break, is characterized by darkening of the nodes and by the ease with which stems break. It was initially described by Luke, Wallace and Chapman (1957) and Jones and Clifford (1983), and observed, in Brazil, by Rocha (1996). These symptoms start appearing from lesions on the leaf sheaths that are in direct contact with the nodes, become dark and make a more severe infection process. When infection is more severe, a mycelial mass of fungus can be seen in the stem cavity, and the stem breaks easily between the third and fourth internodes. These authors emphasize that this blackstem symptom resembles one described for Septoria avenae Frank (Luke, Wallace and Chapman, 1957).
Figure 12.3
Symtoms of oat kernel darkening
produced by the mycelium of Pyrenophora chaetomioides, the causal agent
of Leaf blotch on oat, growing superficially
Besides the symptoms described above, other symptoms can be associated with P. chaetomioides, such as the "spikelet- drop" described by Ivanoff (1963), and spots on stems, which can be elongated and narrow or expand themselves irregularly (Harder and Haber, 1992).
Symptoms on seeds were first described by Blum (1997). Later Bocchese et al. (2001) described symptoms of widespread darkening on the surface of the grain (Figure 12.3), on the three superficial layers of the caryopsis, whose intensity varied from yellow-brown to black, depending on the density of the mycelium and its local enzymatic activity.
On infected crop residues of the host, P. chaetomioides develops structures called pseudothecia, which have often been found on residues of oat crops on farms in the south of Brazil (Martinelli et al., 2003). However, the sexual stage of the fungus (P. chaetomioides) is rarely mentioned in the literature and is considered to be of minor importance as an inoculum source. The asexual form of P. chaetomioides produces conidia on dead straw, which are the main source of inoculum for the forming grains and for subsequent oat crops, since the fungus is not a natural inhabitant of the soil (Shaner, 1981) and it does not survive as resting spores on the soil nor does it have resistant structures (Reis, 1987).
Seeds, in contrast, guarantee the survival of the pathogen for long periods in the absence of other sources of inoculum. According to Machcek and Wallace (1952), recovery of the fungus was possible in 10 percent of oat seeds stored for 10 years, which confirms the importance of infection by the mycelium. In oat seeds stored in a laboratory, Sheridan and Tan (1973) observed that the mycelium of P. chaetomioides stayed viable for seven years. The fungus survives in stored, infected seeds and stays dormant due to the low humidity of the seed, usually from 12 to 13 percent (Reis, 1988).
Shaner (1981) also reported that seeds could be sources of primary inoculum in areas where crop rotation is practiced. The amount of this inoculum will depend on the intensity and on the environmental conditions during the production of the seeds. After sowing, upon germination and emergence of oat seedlings, the mycelium recovers its activity, attacking the first leaf on which the fungus can produce some spores (Reis, 1987). However, the greatest conidia production happens on dead tissues of the basal leaves, forming the secondary inoculum, which is then disseminated to other, more distant, parts of the plant, especially panicles and their forming seeds (Rosa et al., 2003), thus completing its biological cycle. According to Blum (1997), there are no reports of secondary hosts that this fungus can infect to produce inoculum.
Therefore, undecomposed, infected crop residues of infected oats, as well as volunteer plants are important sources of primary inocula for P. chaetomioides. This is accentuated in areas of monoculture or no-till planting, due to reintroduction of the pathogen to the recently established area (Shaner, 1981; Reis, 1987, 1988).
The spread of P. chaetomioides mainly occurs through infected seed (the main source of inoculum) in areas where crop rotation is used. Spread through conidia and ascospores occurs over short distances by wind or through water splashes (Shaner, 1981).
Infection of the seed happens during flowering of the spikelet. Conidia of P. chaetomioides germinate and penetrate the pericarp of the maturing grain. Some works demonstrate that the milk stage is most susceptible to infection and that foliar and seed susceptibility are not connected (Turner and Millard, 1931; Schilder and Bergstrom, 1994). Its viability lasts for a long time (Turner and Millard, 1931).
One of the most desirable methods of control is through genetic resistance. Surveys of this disease exist around the world, such as the European Oat Disease Nursery, which monitors disease incidence and records the effect of the sources of resistance for all important diseases of oats in 19 European countries, as well as Israel and Morocco. This programme has reference sources of resistance to P. chaetomioides, such as those in the oat genotypes Maldwyn, IL86-4189 and IL85- 6467 (Harder and Haber, 1992; Frank and Christ, 1988; Sabesta et al., 1996).
In Brazil, the Federal University of Rio Grande do Sul has been involved in a research programme to select resistant genotypes, characterize their expression and inheritance, and transfer resistance to new cultivars. Recent data (Bocchese et al., 2001) suggest that the resistance that operates in these genotypes is of a quantitative type.
Crop management aiming to reduce the incidence or severity of this disease is based on the reduction of the inoculum at primary sites, which are crop residues of oats, infected volunteer plants and infected seeds (Reis and Casa, 1998). In areas where the inoculum is present on dead matter on the soil surface, crop rotation using non-host species has been the preferred control measure, as well as other practices that eliminate crop residues on the surface of the soil (Shaner, 1981; Reis, 1987; Haber and Hader, 1992).
Control through biological methods must be effective at the rhizosphere level. Inoculation of seeds with antagonistic organisms is more effective in protected situations. In the field, behaviour against the pathogen will depend on its interaction with soil micro-organisms and also with the predominant environment (Maude, 1998). In 1994, Ronquist reported treating oat seeds with isolates of Pseudomonas chloraphis, a common bacterium of the rhizosphere, which gave positive results in the control of Pyrenophora chaetomioides.
Fungicidal seed dressing has been one of the measures most used to control P. chaetomioides (Boewe, 1960; Tempe, 1964; Jones and Clifford, 1983; Hader and Haber, 1992), but treatment with modern fungicides has not been eradicative (Blum, 1997) due to the high level of incidence of the pathogen in the seeds, and, as a consequence, an inability to prevent the spread of the disease to the aerial part of plants. Reis and Soares (1995) tested fungicides and doses to be recommended for seed treatment, and obtained a maximum control of only 30 percent for P. chaetomioides, using a thiram+carboxim mixture. This shows the difficulty of eradicating the fungus by this method.
Scab or Fusarium head blight (FHB) is caused mainly by Fusarium graminearum (teleomorph = Gibberella zeae Schwabe Petch.) (Schoroeder and Christensen, 1963). Other species, such as Fusarium culmorum, F. avenaceum, F. moniliforme, F. oxysporum, F. poae and Microdochium nivale, can also constitute a complex with the disease, although they are usually less important than F. graminearum (Warren and Kommedahl, 1973; Wiese, 1987). Isolates of F. graminearum differ in virulence and there is no evidence of the existence of stable races of the pathogen (Bai, Shaner and Ohm, 1991; Mesterhazy, 1987). Disease caused by F. graminearum is common in areas of humid climate, such as in South America. Its occurrence has increased in recent years, reaching epidemic levels in several countries, including Argentina, Brazil, Canada, Mexico, Uruguay and USA (Reis, Panisson and Boller, 2002).
The causal agent of scab passes part of its life cycle as a saprophyte, decomposing the organic matter of its hosts, which include wheat, barley, rye, triticale, ryegrass, maize and oats, which remain on the surface of the soil. Direct seed drilling or minimum tillage has contributed to the increase of inoculum and the intensity of the disease in the main areas of the world where these cereals are grown. As a consequence, particularly from the mid-1990s, scab emerged as an important pathogen on other species as well, previously considered as non-hosts. For example, in 1999, Martinelli, Mundstock and Federizi reported for the first time the occurrence of an epidemic of F. graminearum on oats in the south of Brazil, although the damage was not precisely estimated at the time.
Figure 12.4
Symptoms of Oat scab (Fusarium head
blight) on crown of oats, caused by the fungus Fusarium
graminearum
For the other cereals, damage caused by the disease can be direct, related to yield losses, or indirect, related to the contamination of grain with mycotoxins produced by the fungus (Sutton, 1982; Parry, Jenkinson and McLeod, 1995; Jones and Mirocha, 1999). In South America, the greatest damage recorded in wheat was 14 percent, with an average of 5.4 percent from 1984 to 1994 (Reis et al., 1996). In the epidemic in 2000, the incidence of scab on wheat was over 70 percent, with yield losses of 14 percent (Panisson, Reis and Boller, 2003).
The characteristic symptoms of scab in oats (Figure 12.4) are discoloured spikelets, pale or whitish in colour, which contrast with normal green healthy panicles. In favourable conditions for the disease, salmon-pink signs of the pathogen are easily observed on infected spikelets, as well as at the base and edges of the glumes. In infected panicles, the grains are light, wrinkled and wilted, with a white-rosy or pale-brown colour.
Warm and humid environmental conditions, such as temperatures between 20 and 25ºC and atmospheric relative humidity higher than 90 percent, or rain for at least 48 hours, favour the disease. Initial inoculum comes from crop remains of several hosts, where the pathogen can survive. The ascospores are disseminated by the wind to the anthers, which are their preferred sites of infection (Reis, Panisson and Boller, 2002).
Scab control is difficult due to the absence of resistance and lack of effective management practices that help reduce the inoculum. Although spores are present on seeds, these are not the main source of inoculum for the establishment of the disease. In addition, none of the fungicides available today are effective as seed dressing, and are not recommended for control of the disease.
Smut diseases, caused by Ustilago spp., which occur worldwide, have been among the most destructive of oat diseases. Until the 1940s, annual losses due to loose smut across the USA were estimated at 3 to 5 percent, and in western Canada losses of 10 to 25 percent were common, with some fields showing 75 percent smutted heads. Despite the use of resistant cultivars and chemical control to reduce disease levels, loose smut occurs most years in many areas. Until a few decades ago, considerable damage occurred in parts of USSR, and an increase in loose smut has been noted in New Zealand (Harder and Haber, 1992). In South America, smut is of minor importance in reducing yields. Its frequency is very low since most fungicides used to control other seed-borne pathogens also control smuts. The disease does not produce any toxic compound, which makes its occurrence less worrying for farmers.
On oats, there are two forms of smut: loose, caused by Ustilago avenae (Pers.) Rostr., and covered, caused by Ustilago kolleri Wille (Wallwork, 1992). Infected plants may be somewhat shorter than healthy ones, but smut symptoms are mainly visible on the panicle. Infected panicles emerge at the same time as healthy ones and usually have a narrower and erect habit. Loose smut destroys seeds, hulls and glumes and replaces them with a powdery mass of dark brown spots. As the crops ripens, most of the spores are blown away or washed off by rain, leaving only a few spores and small, light-grey fragments of host tissue on the panicle. In covered smut, the somewhat compacted spores are enclosed in the remains of hulls and glumes, which turn a light grey towards maturity (Martens, Seaman and Atkinson, 1985).
Oat smuts are carried over from season to season as seed-borne spores. Those lodged under the hull are the most effective in causing new infection. When infected seed is sown, the spores germinate and the hyphae penetrate the very young seedling and invade the growing point. The fungus and host plant develop together until finally the smut destroys the flowers and replaces seeds and most of the glumes with spores. The spores of loose smut are easily dispersed by wind; if they land in healthy florets they complete the disease cycle. Covered smut re-infects in the same manner, but the spores are more often dispersed during grain harvest and handling (Martens, Seaman and Atkinson, 1985).
Under natural conditions, the amount of smut infection varies considerably from year to year, variation depending less on the amount of inoculum available than on the conditions prevailing at flowering or during germination. Spore release peaks to coincide with flowering (Mills, 1967), but cool, dull conditions at flowering may result in less opening of the florets, and hence less opportunity for floral infection. Smut fungi tolerate relatively wide ranges of temperatures and humidity, but the amount of infection is strongly influenced by interactions of factors that affect germination and growth of both fungus and host. In general, infection occurs between 6 and 25°C, with an optimum of around 18 to 22°C, provided that soil moisture is relatively low. High soil temperature combined with high moisture is least favourable for infection (Harder and Haber, 1992).
Smut control is now relatively easy because either systemic fungicides (Martinelli, 1998; von Schmeling and Kulka, 1966) or breeding for resistance are effective since more varied sources of resistance have been found in breeding programmes (McKenzie et al., 1981, 1984).
Since the mid-1980s, barley yellow dwarf has become increasingly widespread in the USA and is now of serious concern to oat and wheat producers. Outbreaks occasionally reach epidemic proportions, as occurred on wheat in 1987 and oats in 1988.
Barley yellow dwarf virus (BYDV) is a member of the luteovirus group. Luteoviruses are characterized by inducing "yellowing" symptoms and are restricted to phloem and thus not mechanically transmissible; they are persistently and specifically transmitted by aphids, and occur as about 25-nm isometric particles (Mathews, 1982). BYDV actually includes several related viruses, grouped into five strains based primarily on the specific aphid species able to transmit a particular strain. BYDV can be transmitted by 23 species of aphid and infects almost 100 species of annual and perennial grasses, including barley, maize, oats, rye and wheat (Watkins and Lane, 2004).
BYD is diagnosed (Figure 12.5) in the field by the presence of yellowish to reddish stunted plants grouped singly or in small patches among normal plants. Early infection of any of the cereals may result in severe stunting, excessive or reduced tillering, bright-yellowing or reddening of older leaves, delayed heading or ripening, increased sterility, and fewer and lighter kernels. In some oat cultivars, leaves become bronzed. This disease is not the only cause of red coloration in oats. Post-seedling infections are progressively less severe to the point where only the upper leaves, or the flag leaves, show discoloration. The leaves of plants infected with BYDV are shorter than normal and the flag leaf may be severely shortened. Leaves are often stiffer and more erect. Root systems are reduced and diseased plants are more easily pulled up than healthy ones (Wallwork, 1992; Watkins and Lane, 2004). On oats the first symptoms are yellowish-green spots or blotches near the tips of older leaves. Eventually these blotches enlarge and coalesce. Symptoms vary according to the variety, the virus strain, the growth stage of the plant at the time of infection, the general health of the plant, the temperature and other environmental factors. The main colour change is to shades of yellow, reddish-orange, reddish-brown, or purple (Martens, Seaman and Atkinson, 1985).
Stunted plants result from the failure of stem internodes to elongate. This leads to a "telescoped" plant where the leaves may unfurl before they have fully emerged from the sheath of the previous leaf. Infected plants are "dwarfs" and have lost their normal conformation. Even the panicle fails to emerge fully or properly. Patterns of BYD in a field may be seen either as random within the crop or as circular or angular patches, which reflect the pattern of movement of the aphid vectors or carriers. Many infected plants ripen prematurely, after which they may be invaded by sooty moulds, which give them a dirty appearance and may lower germination of harvested seed (Watkins and Lane, 2004).
Figure 12.5
Symptoms of Barley Yellow Dwarf Virus
(BYDV) on oats
Of the more than 20 aphid species that transmit BYDV, the most important are the oat bird-cherry aphid (Rhopalosiphum padi), maize leaf aphid (Rhopalosiphum maidis), English grain aphid (Sitobion avenae), and the greenbug (Schizaphis graminum). The rose grass aphid (Metapolophium dirhodum) is widespread in Europe but not in North America. The oat bird-cherry and the English grain aphids are the most important carriers of BYDV in oats.
BYDV overwinters in infected winter cereals and in wild and cultivated grasses. Perennial grasses such as bluegrass (Poa pratensis L.), cocksfoot (Dactylis glomerata L.), tall fescue (Festuca arundinacea Schreb) and little bluestem (Andropogon scoparius Mixch) may serve as reservoirs of the various strains of BYDV. Oats and barley are very susceptible to BYDV. Where these crops are sown late for soil cover, wind erosion control, for fodder, or are volunteers, they are often heavily infected and can be an important local source for migration of aphids and the virus into adjacent autumn sown wheat.
Aphids acquire BYDV by feeding on infected plants. It normally takes 24 to 48 hours of feeding to acquire the virus, but, once done, the aphid remains a carrier for life. Spread of BYDV depends entirely on aphid movement. One very active aphid feeding for short periods on different plants is a more important carrier than several stationary ones.
Damaging outbreaks of BYD are most likely at high light intensities and in cool, moist seasons (near 15°C), which favour not only grass and cereal growth but also aphid reproduction and migration. Driving rain may spread aphids, but will also reduce their populations. BYDV is specialized in its relationship with aphid carriers and is not transmissible through seed, plant sap or other insects (Harder and Haber, 1992; Watkins and Lane, 2004).
The best control is based on varietal resistance or tolerance. Resistance or tolerance is available in barley and oats. The oat cultivars Bates, Hazel, Noble, Otee and Pierce are resistant to BYD; Don, Lang, Larry, Ogle, Starter and Steele are moderately resistant.
Late-planted spring oats in the North Hemisphere and early-planted oats in South America are most susceptible to infection. Younger plants are more attractive to aphids than older ones. To minimize outbreaks, sowing of winter cereals should be delayed until aphid populations decline. Proper sowing date allows the plants to develop when aphid populations are lowest. In addition, seed treatment with insecticides, such as Imidacloprid (for Schizaphis graminum) or Thiamethoxam (for Metopolophium dirhodum), or both, may contribute to reduce the levels of aphids at early stages of development of the plant (up to 60 days after germination).
Bacterial blight has been reported from most regions of the world where oats are grown. It is usually not a serious economic threat, but may cause considerable damage under some conditions. The disease poses a greater problem in relatively cool, moist areas, such as the British Isles (Davies, Noble and Norman, 1955), the Highlands of Kenya (Harder and Harris, 1973), on winter oat in Canada (Martens, Seaman and Atkinson, 1985) and in the southeastern USA (Cheng and Roane, 1968), or in some winters in South America (personal observation of the author).
Halo blight of oats is caused by Pseudomonas coronafaciens (Elliot) Young, Dye, Wilkie. Lesions occur mainly on leaf blades, but they are also found on stems, coleoptiles and leaf sheaths. Halo blight produces light green, oval spots, the centres of which become water-soaked and darker than the margins. Spots seem to be surrounded by pale green halos. Later, the whole spot, including the halo, turns brown. Spots may coalesce to form an irregular blotch. There are usually little bacterial exudates from the lesions. Exceptionally, if conditions remain particularly favourable, the entire plant may be defoliated, or the bacteria may reach the crown, killing the plants (Martens, Seaman and Atkinson, 1985; Harder and Haber, 1992; Wallwork, 1992).
Bacteria causing halo blight are seedborne and can survive on infected crop residues. The first seedling infections develop from bacteria on the surface of the seeds. From these infections, the bacteria can spread readily from leaf to leaf and from plant to plant during moist spring weather. In late spring, the disease in some fields may look severe, but often a spell of warm, dry weather will check the development of blight and new growth will be relatively free from infection. During the growing season, infection takes place through pores at the tips of the leaves, through stomata distributed over the surface of the leaves, and through wounds. Rain, wind and insects, particularly aphids, are the agents responsible for disease spread (Martens, Seaman and Atkinson, 1985; Wallwork, 1992).
Figure 12.6
Septoria blotch on oats, caused by
the fungus Septoria avenae f.sp. avenae (perfect state Phaeosphaeria
[Leptosphaeria] avenaria f.sp. avenaria O.E.
Erikss)
In most temperate regions, specific measures are not usually necessary as little further spread of bacteria occurs with the advent of higher summer temperatures. In circumstances where the disease may cause economic losses, cultural methods, such as use of clean seed and avoidance of infected oat debris, should reduce disease levels. Resistance to halo blight is effective and simply inherited. Thus, it should not be difficult to breed resistant cultivars (Harder and Haber, 1992; Wallwork, 1992; Martens, Seaman and Atkinson, 1985).
Septoria disease of oats is caused by the fungus Septoria avenae f.sp. avenae (perfect state Phaeosphaeria [Leptosphaeria] Avenaria f.sp. Avenaria). Other common names for the disease are Septoria leaf blotch (Figure 12.6), speckled leaf blotch, and Septoria black stem. In cool, moist seasons this is one of the most destructive diseases of oats in the northern third of Illinois, USA (Babadoost, 2004).
Up to 93 percent of the leaves and 31 percent of the nodes have been found infected in an Illinois oat field. Almost 20 percent of the leaf area was killed. The black-stem phase of the disease had killed many of the culms above the top joints, causing severe lodging. Statewide yield losses of 15 percent or more have been recorded in the major oat-producing states of the Midwest and Northeast USA and in Canada. In Canada it is usually of minor importance in western Canada, but it can be particularly severe in eastern Quebec and parts of the Maritime Provinces, where cool, humid weather and a long growing season prevail (Martens, Seaman and Atkinson, 1985; Babadoost, 2004). In Australia, yield losses of 30 percent have been recorded due to Septoria blotch (Wallwork, 1992). Generally, the disease is sporadic in its occurrence from season to season and from area to area. Septoria blotch has not yet been recorded in south Brazil.
Septoria fungus is capable of attacking all aboveground portions of the oat plant at most stages in its development. Under appropriate environmental conditions, characteristic leaf, leaf sheath, culm, glume and kernel infections are produced. Leaf infections and culm breakage reduce yields and cause lodging. Kernel infections reduce milling quality. Infected straw may have reduced feeding value.
The symptoms of the disease are small, dark brown to purple, oval or elongated spots on leaves. These spots grow into larger light or dark brown blotches up to 20 mm in diameter, with surrounding yellow areas that can cover and kill the entire leaf. The infection may spread to leaf sheaths and through them to stems, where greyish brown or shiny black lesions form. Severe infection may cause lodging. Dark brown blotches can also occur on the head and grain. It is possible sometimes to see tiny black specks (fruiting bodies) in the centre of older blotches (Wallwork, 1992).
The causal fungus overwinters in plant refuse and stubble of a previous oat crop. The sexual stage of the fungus develops in the spring on the refuse and stubble, and produces ascospores that infect leaves of the new crop at about the boot stage. As infection spreads and lesions enlarge, the asexual stage of the fungus develops and produces pycnidiospores, which continue the secondary spread of the disease, especially in humid weather. When infection is severe, leaves senesce early and stems became black, weakened and broken. When lodging occurs, seed yield losses may average 25 percent and seed weight and quality are reduced (Martens, Seaman and Atkinson, 1985).
Oat cultivars and selections differ in their resistance to Septoria blotch. According to Babadoost (2004), earlymaturing cultivars tend to be most susceptible. Tall, late cultivars are generally more resistant or escape infection. More resistant cultivars should be available in the future. The wild diploid Avena species (e.g. A. brevis, A. nudibrevis, A. strigosa and A. wiestii) appear to have considerably more resistance than A. sativa. These species may serve as sources of resistance to this disease. Reaction to Septoria is a quantitative character and segregating populations can not be separated into clear-cut classes. Septoria reaction is also influenced by differences in the environment. Oat cultivars and selections also differ in their reaction to all phases of the disease - leaves, culms, glumes and kernels. Resistance to one phase, however, tends to be associated with resistance to other phases.
Powdery mildew
On oats, the symptoms of this disease are very similar to the other cereals (Martinelli, 2001). Initially, they appear as colonies of fluffy white to light grey superficial mycelium, on the upper surfaces of the leaf blades. Sheaths and spikes can be affected under favourable conditions. The mycelium darkens to a yellowish grey with age. The undersides of affected leaves have yellowish necrotic spots at infection sites. At this stage, dry powdery conidia are produced in abundance. Late in the season, black spherical fruiting structures (cleistothecia) develop in the mycelial mats. The fungus (Blumeria graminis f.sp. avenae) is biotrophic and therefore attacks only living cells (Zillinsky, 1983; Martinelli, 1990). The disease is favoured mainly by cold, dry springs. On oats, it has been considered a disease of minor importance. To control it, the use of resistant cultivars is the best and most effective approach. Chemical seed treatment can be effective (Martinelli, 2001).
Ergot
Ergot is usually considered a disease of rye, but can attack other cereals, including oats, barley, wheat and many grasses. The fungus (Claviceps purpurea) only attacks seed-producing organs and generally yield losses are less serious than losses from discounted grain quality. The ergot bodies (sclerotia) that replace the kernels are toxic to humans and animals, and are difficult to remove from harvested grain (Zillinsky, 1983).
Ergot is more prevalent in cool, temperate climates. The prevalence of the disease may be related to the susceptibility of native grasses in these areas. Flowering habits and floral structures may compromise the level of incidence of the disease (Zillinsky, 1983).
Nematode damage
The cereal cyst nematode (CCN; Heterodera avenae) has been reported in many countries. Light soils are generally favourable to it, although with continuous cereal cropping it will generally cause economic damage, irrespective of soil type. Distribution of damage within a field is often uneven. Infestation by the cereal cyst nematode results in a stunted, knotted root system. Aerial parts show reduced growth and yellowed leaves. Panicle development is delayed or absent in severe infestations. Moist, cool weather at the time of larval emergence is favourable to the nematode (Araya and Foster, 1992).
The stem nematode, Ditylenchus dipsaci, is widespread throughout western and central Europe, North and South America, Australia and North and southern Africa. The nematode invades the foliage and the stem base of cereals, causing a breakdown of the middle lamellae between cells by secreting a pectinase. The nematodes are highly mobile in moist, sandy soil and can spread rapidly from one plant to another. Nematode activity is greatly decreased in well-drained fields (Araya and Foster, 1992).
In many areas of the world, the importance of the diseases on fodder oats has been neglected by many involved in their production, such as governments, technicians and even farmers. In this sense, the impact of the diseases in those areas has been partially underestimated, mainly because they do not affect a product that is directly consumed by man. Nevertheless, the damage has often been serious. Often farmers’ lack of information and precarious technical support has hindered control, or appropriate management, to avoid losses.
Nowadays, most of the information on oat diseases, their biological characteristics, epidemiology and genetics, originates from research on oats destined for the production of grain. Most of the data is, therefore, less appropriate to fodder production since it has different scale levels, different management and a different environment. In the same way, breeding programmes have concentrated on obtaining resistance for diseases of oats destined for production of grain, especially the rusts, with less emphasis on BYDV, Pyrenophora leaf blotch and Septoria.
Certainly, there is a demand for more detailed information about the impact of diseases on fodder oats. All aspects of the interaction of the pathogens with oats, particularly in their natural environment, need to be better understood so that efficient control mechanisms can be developed. Therefore, there is now a considerable demand for a search for and transfer of genetic resistance to most of the diseases that occur on oat species used as fodder.
Recently, some oat breeding programmes have realized this need and begun to make selections and crosses aimed at obtaining more adapted, productive and resistant varieties. Although some small steps have been taken, much still needs to be done. With respect to diseases, fodder oats need require high levels of resistance and, ideally, should not need fungicidal sprays. Challenges such as crown and stem rusts have been difficult to overcome, particularly in favourable environments. Resistance to new and more complex diseases, like scab, will need much more research and investment.
In the authors’ opinion, the importance that fodder oats have assumed in the world is unquestionable due to their huge area and economic impact. This fact itself should certainly influence public institutions and funding bodies to allocate resources to decreasing the impact of diseases. Modern molecular and cellular techniques, such as tissue culture and recombinant DNA, offer a promising route to achieving this goal. In this field, progress would be achieved faster were the various activities of government agencies, the private sector and scientific communities to become even more harmonized.
