Blumeria graminis (powdery mildew of grasses and cereals)
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Seedborne Aspects
- Plant Trade
- Detection and Inspection
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Blumeria graminis (DC.) Speer
Preferred Common Name
- powdery mildew of grasses and cereals
Other Scientific Names
- Erysiphe graminis DC.
- Oidium monilioides (Nees) Link
International Common Names
- Spanish: cenicilla de los cereales; oidio de los cereales
- French: blanc des cereales; blanc des graminees; oidium des cereales
Local Common Names
- Germany: Mehltau: Getreide
- ERYSGR (Blumeria graminis)
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Ascomycota
- Subphylum: Pezizomycotina
- Class: Leotiomycetes
- Order: Erysiphales
- Family: Erysiphaceae
- Genus: Blumeria
- Species: Blumeria graminis
Notes on Taxonomy and NomenclatureTop of page
This fungus is the only species of the genus Blumeria but it has previously been treated as a species of Erysiphe. According to Braun (1987), it differs from all species of Erysiphe because its anamorph possesses unique features, for example, digitate haustoria, secondary mycelium with bristle-like hyphae and bulbous swellings of the conidiophores, and because of the structure of the ascocarps. Braun (1987) considers that, because of these differences, there should be a separation at generic level. Molecular sequence analyses proved the separate position of the powdery mildew on Poaceae and showed that Blumeria takes a basal position in the phylogenetic trees of the Erysiphales. Hence, Blumeria is only distantly related to Erysiphe and all other genera of the powdery mildew fungi (Saenz and Taylor, 1999; Mori et al., 2000; Braun et al., 2002).
As a biotrophic parasite, B. graminis has evolved to specialize on particular poaceous hosts. Traditionally, eight special forms or formae speciales of B. graminis were identified. They were ff. spp. tritici (Triticum and Aegilops spp.), hordei (Hordeum), avenae (Avena sativa), secalis (Secale cereale), agropyri (Agropyron and Elymus), bromi (Bromus spp.), poae (Poa spp.) and dactylidis (Dactylis spp.). The adaptation of B. graminis to specific cereal hosts involves both pathogen-associated molecular pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) and has been termed ‘non-adapted resistance’ (Troch et al., 2014). This adaptation is strong enough that B. graminis f.sp. tritici does not parasitize domesticated barley, and B. graminis f.sp. hordei does not infect wheat.
B. graminis continues to evolve, and new formae speciales can arise. For example, starting in 2001 in France, B. graminis was found on triticale (X Triticosecale), a wheat-rye hybrid (Walker et al., 2011). The new strains were themselves a hybrid of B. graminis ff. spp. tritici and secalis, and have been called f.sp. triticale ( Troch et al., 2012; Menardo et al., 2016), which makes nine ff.spp. In the Middle Eastern centre of origin of the pathogen, B. graminis f.sp. tritici is significantly differentiated into populations primarily infecting tetraploid wild emmer or hexaploid domesticated wheat; however, it is unclear that the evidence supports the existence of a tenth forma specialis specialized on tetraploid wheats (Ben-David et al., 2016; Menardo et al., 2016).
It has been proposed that the forma specialis concept should no longer be applied to B. graminis from most wild grasses, where the tight association between evolution and host-specialization evident on domesticated cereal hosts does not exist (Troch et al., 2014). If adopted, this proposal would retain the formae speciales tritici, hordei, secalis, avenae and triticalis for the B. graminis strains specialized on the agricultural crops of wheat, barley, rye, cultivated oat (A. sativa) and triticale, respectively. But the f.sp. concept would no longer be applied to B. graminis from wild grasses; instead, the host species of origin would simply be mentioned when necessary to clarify the origin of an isolate.
DescriptionTop of page
See also Kapoor (1967) and Braun (1987, 1995).
DistributionTop of page
Powdery mildew of cereals and grasses has a genuinely worldwide distribution (Cowger et al., 2012). B. graminis is distributed widely in Europe, North America, central Asia, and China. In addition, powdery mildew of wheat also occurs in Egypt, the Western Cape of South Africa, the higher-rainfall areas of Western Australia, and parts of Latin America (e.g., southern Brazil).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 25 Feb 2021
Risk of IntroductionTop of page
Hosts/Species AffectedTop of page
Host Plants and Other Plants AffectedTop of page
|Avena sativa (oats)||Poaceae||Main|
|Bromus catharticus (prairiegrass)||Poaceae||Other|
|Elymus smithii (Colorado bluestem)||Poaceae||Other|
|Festuca arundinacea (tall fescue)||Poaceae||Other|
|Hordeum vulgare (barley)||Poaceae||Main|
|Lolium perenne (perennial ryegrass)||Poaceae||Main|
|Phalaris paradoxa (awned canary-grass)||Poaceae||Other|
|Poa pratensis (smooth meadow-grass)||Poaceae||Other|
|Poaceae (grasses)||Poaceae||Wild host|
|Secale cereale (rye)||Poaceae||Main|
|Triticum aestivum (wheat)||Poaceae||Main|
|Triticum turgidum (durum wheat)||Poaceae||Main|
Growth StagesTop of page
SymptomsTop of page
Powdery mildew appears in the form of white, later grey-tan areas on all aerial parts of cereals and grasses i.e. leaves, stems and ears, although leaves are most commonly infected. Initial symptoms are easily overlooked and take the form of chlorotic flecks on plant tissue. This is quickly followed by the development of white, beige or grey patches which produce masses of conidia (asexual spores) and assume a powdery appearance. If the plant is shaken even gently, clouds of conidia are released from the patches. Ascomata (fruit bodies forming sexual spores, termed chasmothecia) may or may not form, but when they do, they occur late in the season and can be found embedded in the mildew colonies as tiny, dark-coloured dots.
List of Symptoms/SignsTop of page
|Inflorescence / lesions on glumes|
|Leaves / abnormal colours|
|Leaves / fungal growth|
|Roots / reduced root system|
|Stems / mycelium present|
Biology and EcologyTop of page
B. graminis bridges the gap between host crops mainly as a mycelial mat on leaves of grasses and autumn-sown cereals. The ascomata (chasmothecia) produced during the late spring or summer in that mycelial mat are fairly resistant to temperature extremes and to drying out, and are thus an important source of inoculum for the next season. In humid weather, chasmothecia release ascospores which can start infections on autumn-sown crops in the autumn and perhaps also in the spring. As temperatures rise in the spring, dormant mycelium commences growth and conidia are produced rapidly. Conidia usually germinate over a range of temperatures from about 3 to 31°C, although 15°C is probably optimal for germination, together with a relative humidity about 95%. Conidial germination is inhibited by free water. Under favourable conditions, fresh conidia can be found in about 7 days and are dispersed within the crop and further afield in the wind. Crucially, therefore, epidemics of powdery mildew will tend to occur during conditions of alternating wet and dry weather, with some wind to ensure dispersal of the conidia.
Mildew is encouraged by very early autumn sowing, especially in barley. In the autumn, heavily infected plants may be less resistant to winter frosts and plants may die. Powdery mildew is also encouraged by excessive use of nitrogen fertilizer and can be particularly severe in dense crops grown in a sheltered, humid environment. The planting of highly susceptible cultivars is a prime reason that powdery mildew becomes an economic problem in areas where it was previously scarce.
Seedborne AspectsTop of page
Seed treatment with difenoconazole, followed by flutriafol, triticonazole and triadimenol was shown to achieve the highest fungal protection in wheat (Reis et al., 2008).
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Flowers/Inflorescences/Cones/Calyx||fungi/hyphae; fungi/spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Leaves||fungi/hyphae; fungi/spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Stems (above ground)/Shoots/Trunks/Branches||fungi/hyphae; fungi/spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Plant parts not known to carry the pest in trade/transport|
|Fruits (inc. pods)|
|Growing medium accompanying plants|
|True seeds (inc. grain)|
ImpactTop of page
Powdery mildew is one of the most common and destructive diseases of cereals. Actual losses depend on the time of disease epidemic onset and its severity, and can at the extreme reach up to 60% (James et al., 1991; Oerke et al., 1994). Although it occurs in most, if not all, parts of the world where cereals are grown, powdery mildew is not considered to be a major problem in every region. This disease can be very destructive, but generally seems to cause most damage in temperate latitudes, especially in the northern hemisphere, where wheat and barley are more frequently cultivated (see map in Cowger et al., 2012). However, powdery mildew can also be a limiting factor for cereal production in subtropical and tropical areas. Yield losses by powdery mildews are generally complex to estimate and depend on several factors such as climate, year, cropping system, cereal species and cultivar.
In some parts of Europe, powdery mildews are a limiting factor to the yield of cereals. In the UK, powdery mildew is considered a moderate risk for wheat growers, with 13-17% of crops affected in the 2014-2015 period (AHDB, 2016). Powdery mildew generally reduces wheat yields less than other foliar diseases, with yield losses due to wheat powdery mildew rarely exceeding 10% in the UK. Scottish spring barley has seen an increase in powdery mildew in recent years due to widespread planting of a highly susceptible malting variety (FAS, 2019).
Powdery mildew is a major wheat disease in northern and central Europe (Miedaner and Flath, 2007). Also in barley production in central and north-western Europe, including the Czech Republic, powdery mildew can be an important constraint (Dreiseitl, 2011). Specific estimates of yield impact in this region are not recent. Field trials with winter barley in Germany between 1975 and 1981 revealed yield losses of 11% due to powdery mildew (Kolbe, 1982). Despite the use of crop protection measures, Lutze et al. (1982) calculated that the average yield loss due to powdery mildew over 6 years was 5.3% (a range of 3.3 to 6.2% was estimated) in barley cultivated in the east of Germany. Based on a yield level of 7.5 t/ha, heavy infections by powdery mildew resulted in losses of 4.8% in wheat during 1969-79 in Germany (Anderl et al., 1984). In the Czech Republic, yield losses of 17% were reported in wheat growing under a severe infection pressure of powdery mildew (Benada and Vanova, 1984). In Romania, crop losses due to B. graminis f.sp. tritici varied from 1 to more than 20% depending on the region in which it occurred (Ciurdarescu et al., 1987).
Wheat powdery mildew occurs frequently in the eastern states of the USA; severe epidemics occur most often in the mid-Atlantic region, although widespread planting of susceptible cultivars has caused outbreaks from Georgia to Oklahoma to Montana (Cowger et al., 2018). Estimates of yield losses in susceptible cultivars ranged from 12 to 20% in Virginia (Griffey et al., 1993) and decreases of up to 30% in number of tillers and kernels per head were observed from early-onset epidemics in North Carolina (Bowen et al., 1991). In Kentucky, USA, an average yield loss of 20% was associated with powdery mildew over two experimental years in soft red winter wheat (Pearce et al., 1996).
Among the pathogens of wheat in Argentina, powdery mildew practically occurs every year in the wheat cropping area, particularly in the first growth stages and less frequently in later stages (Molteni et al., 1996). In general, it is not economically important in the crop area of La Pampa Humeda, in contrast to areas with higher temperatures such as Santa Fe, Entre Rios and Chaco, where the disease also occurs at later growth stages and can therefore cause significant yield losses. However, no precise data on losses by powdery mildew are available for wheat in Argentina. In field experiments carried out in the south of Brazil during 1981, powdery mildew reduced the yield of a wheat susceptible cultivar by 8% (Luz, 1984). In 1986, experimental results showed that yield losses attributed to the lack of fungicide control of powdery mildew varied from 20-23% (in susceptible cultivars) to 55% (in a highly susceptible wheat cultivar) (Linhares, 1988).
Based on figures from the Chinese crop protection authorities, Teng (1986) quoted losses nationwide due to powdery mildew in wheat as 3.4%. Wheat powdery mildew has tended to be more severe in China since the late 1970s (Cao et al., 2013) and the disease has spread from south-western China into the eastern and northern regions (Liu et al., 2019). Destructive epidemics in 1990 and 1991 caused yield losses up to 1.44 and 0.77 million tons, respectively (Zou et al., 2018). Over the period 2002-2019, an average of 10 million ha per year of wheat experienced powdery mildew outbreaks in China (Liu et al., 2019).
In New Zealand, Cromey et al. (1992) reported losses in winter wheat of up to 35% due to powdery mildew infection of susceptible cultivars. In Australia, powdery mildew is a major problem for growers in the western region, especially in south-west Western Australia (GRDC, 2012); in that state, recent losses to barley powdery mildew were estimated at $30 million annually. Powdery mildew is the most damaging barley disease in Western Australia (Tucker et al., 2013).
DiagnosisTop of page
Detection and InspectionTop of page
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
Cultural Control and Sanitary Methods
As volunteer cereals act as overwintering sources of inoculum and stubble and crop debris may harbour chasmothecia, eradication of volunteers and disposing of stubble and debris are important aspects of cultural control. Isolation of autumn-sown and spring-sown cereals (i.e. not growing them too close together) will reduce the risk of infection of the autumn-sown crop spreading to the spring-sown crop. In addition, because nitrogen fertilizer promotes lush crop growth and encourages mildew development, excessive use of nitrogen should be avoided.
Host-plant resistance is very important in the control of powdery mildew on cereals. A wide range of resistance to powdery mildew is exhibited by varieties of wheat, barley and oats, and in those countries where mildew is widespread, it is prudent to choose a variety with a good resistance rating. If the variety grown has poor resistance to powdery mildew, careful crop monitoring will be necessary in order to optimise the timing of fungicide applications. In warmer regions, even a moderate amount of host resistance, or adult-plant resistance, is often adequate to make fungicide application unnecessary, because powdery mildew development ceases when day-time high temperatures routinely exceed 26°C.
For control of powdery mildew in areas prone to severe epidemics, a common approach to host resistance has been to deploy one or more Pm genes in a genetic background of relatively strong quantitative resistance. Selection by breeders in areas conducive to powdery mildew epidemics can result in high levels of adult-plant or other partial resistance in regional germplasm, e.g. in Scandinavia (Hysing et al., 2007; Lillemo et al., 2010). As Pm genes can be rapidly overcome if they are widely deployed, new resistance sources have been continuously sought. In the USA, there has been considerable success in introgressing new powdery mildew (Pm) genes into wheat bred for mildew-prone areas. For example, since 1987, 16 new resistance sources were identified in diploid and tetraploid wheat relatives and introgressed into a common soft winter wheat background under the direction of Dr Paul Murphy at North Carolina State University, resulting in five Pm gene and two temporary gene designations (summarized in Cowger et al., 2018). Characterization of novel resistance sources in wheat relatives and landraces is ongoing in China (e.g., Zou et al., 2018) and Oklahoma, USA (summarized in Li et al., 2019).
The strategic deployment of host resistance can be effective against powdery mildew, which is the classic wind-borne polycyclic pathogen. For example, spread of mildew from one field to another can be reduced by the correct diversification of varieties. In the UK, the National Institute of Agricultural Botany (NIAB) produces a leaflet on Diversification Schemes which gives information on good combinations of varieties. Growing mixtures of varieties is also an option to reduce cereal powdery mildew (Chin and Wolfe, 1984; Finckh et al., 1999; Newton et al., 2002).
Fungicides are widely used in the control of powdery mildew in cereals. Chemistries that have been used for control of mildew on wheat and barley include morpholines (e.g., fenpropidin), demethylase inhibitors (DMIs, e.g., tebuconazole and cyproconazole) and quinone outside inhibitor (QoI, or strobilurin) fungicides. Differences in the efficacy of fungicides used in mildew control are due, in large part, to the emergence of isolates of B. graminis that are insensitive to fungicide groups. Reduced efficacy of DMIs and in some cases morpholines against B. graminis f.sp. tritici was observed in the 1980s and 1990s in Europe (e.g., Godet and Limpert, 1998). Widespread resistance to strobilurin fungicides in European B. graminis f.sp. tritici populations appeared starting in the late 1990s, after only 2 to 3 years of use (Chin et al., 2001; Fraaije et al., 2002; Miedaner and Flath, 2007). B. graminis f.sp. tritici was one of the pathogens that most rapidly evolved to QoI insensitivity in Europe (Fisher et al., 2004).
Mildew infection on oats can also be controlled using morpholines and triazoles, although in some countries such as the UK, the range of fungicides approved for oats is limited compared to other cereals. A new fungicide, Falcon 460 EC, containing the new active ingredient spiroxamine, was introduced in Slovenia in 2000 for the control of a range of diseases including powdery mildew on cereals (Kraner, 2001). In addition, simeconazole (2-[4-fluorophenyl)-1-(1H-1,2, 4-triazol-l-yl)3-trimethylsilylpropan-2-01), a novel triazole fungicide with broad spectrum activity was launched as a new seed treatment (Tsuda et al., 2000). It has activity against powdery mildew (B. graminis) and has been shown to increase wheat yields by 10% compared to untreated crops.
In Australia, reduced sensitivity to DMIs has been observed in B. graminis f.sp. hordei (Tucker et al., 2015) and B. graminis f.sp. tritici populations (Lopez and Kay, 2017). A key mutation conferring insensitivity to QoI fungicides was detected in B. graminis f.sp. tritici in 2016 in eastern Australia (Group, 2016).
Fungicide insensitivity is much less evolved in B. graminis f.sp. tritici populations in the USA than in those from Europe or Australia, presumably due to the lesser frequency of fungicide applications. However, eastern US isolates had lower DMI sensitivity than those from the central states, indicating some loss of efficacy (Meyers et al., 2019).
ReferencesTop of page
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Peusha H, Hsam S L K, Ėnno T, Zeller F J, 1996. Identification of powdery mildew resistance genes in common wheat (Triticum aestivum L. em. Thell.) VIII. Cultivars and advanced breeding lines grown in Finland. Hereditas (Landskrona). 124 (1), 91-93. DOI:10.1111/j.1601-5223.1996.00091.x
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Stojanovic S, Stojanovic J, Jevtic R, 1995. Efficacy of barley resistance genes to powdery mildew. In: Zastita-Bilja, 46 183-187.
Sýkora M, Krippel E, Miklovičová M, Plesník S, 1995. Sensitivity of barley powdery mildew (Erysiphe graminis f.sp. hordei) populations against some fungicidal substances in central Europe. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz. 102 (2), 211-214.
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Tucker M A, Moffat C S, Ellwood S R, Tan K C, Jayasena K, Oliver R P, 2015. Development of genetic SSR markers in Blumeria graminis f. sp. hordei and application to isolates from Australia. Plant Pathology. 64 (2), 337-343. DOI:10.1111/ppa.12258
Vikas Gupta, Selvakumar R, Satish Kumar, Mishra C N, Tiwari V, Indu Sharma, 2016. Evaluation and identification of resistance to powdery mildew in Indian wheat varieties under artificially created epiphytotic. Journal of Applied and Natural Science. 8 (2), 565-569. http://jans.ansfoundation.org/previous-issues/volume-8-year-2016-issue-2#TOC-Varieties-and-mulching-influence-on-weed-growth-in-wheat-under-Indo--Gangetic-plain-of-India
Yahyaoui A H, Reinhold M, Scharen A L, 1997. Virulence spectrum in populations of the barley powdery mildew pathogen, Erysiphe graminis f.sp. hordei in Tunisia and Morocco in 1992. Plant Pathology. 46 (1), 139-146. DOI:10.1046/j.1365-3059.1997.d01-11.x
Zhang F L, Zhang Y, Zhang J, Xu K D, Liu K, Wang Y, Lu Y J, Xiang J, Zhang L, Shi X Y, Wang H, Tan G X, Cao P, Li C W, 2014. First report of powdery mildew caused by Blumeria graminis on Festuca arundinacea in China. Plant Disease. 98 (11), 1585-1586. http://apsjournals.apsnet.org/loi/pdis DOI:10.1094/PDIS-06-14-0567-PDN
Zou YaFei, Qiao HongBo, Cao XueRen, Liu Wei, Fan JieRu, Song YuLi, Wang BaoTong, Zhou YiLin, 2018. Regionalization of wheat powdery mildew oversummering in China based on digital elevation. Journal of Integrative Agriculture. 17 (4), 901-910. DOI:10.1016/s2095-3119(17)61851-3
ContributorsTop of page
22/11/19 Reviewed by:
Christina Cowger, Department of Plant Pathology, North Carolina State University, USA
22/11/19 Review of Taxonomy:
James KM Brown, John Innes Centre, Norwich, UK
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