Monilinia fructigena (brown rot)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Habitat List
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Seedborne Aspects
- Pathway Causes
- Pathway Vectors
- Plant Trade
- Impact Summary
- Economic Impact
- Risk and Impact Factors
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Gaps in Knowledge/Research Needs
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Monilinia fructigena Honey ex Whetzel 1945 (teleomorph)
Preferred Common Name
- brown rot
Other Scientific Names
- Acrosporium fructigenum (Pers.) Pers. 1822
- Monilia fructigena Pers.: Fr. 1801 (anamorph)
- Oidium fructigenum Kunze & J. C. Schmidt 1817
- Oidium wallrothii Thüm. 1875
- Oospora candida Wallr. 1833
- Oospora fructigena (Pers.: Fr.) Wallr. 1833
- Sclerotinia fructigena (Pers.: Fr.) J. Schröt. 1893
- Sclerotinia fructigena Aderh. & Ruhland 1905 (anamorph)
- Torula fructigena Pers. 1796
International Common Names
- English: blossom blight; blossom blight of fruit trees; blossom wilt; fruit canker; spur blight; spur canker; twig blight; twig canker; wither tip
- Spanish: momificado; momificado de las frutas; podredumbre de las frutas; pudricion café de la manzana; pudricion café de la pera; pudricion café del chabecano; pudricion café del durazno
- French: brulure des rameaux du cerisier; brulure sclerotique du cerisier; monilia des arbres fruitiers; moniliose des arbres fruitiers; mycose des arbres fruitiers à noyau; pourriture brune des arbres fruitiers; rot-brun des arbres fruitiers
Local Common Names
- Germany: Bluetenduerre: Kern- und Steinobst; Braunfaeule: Kern- und Steinobst; Fruchtfaeule: Kern- und Steinobst; Polsterschimmel: Kern- und Steinobst; Zweigduerre: Kern- und Steinobst; Zweigduerre: Obst
- MONIFG (Monilinia fructigena)
Summary of InvasivenessTop of page
M. fructigena is one of several apothecial ascomycetes causing brown rot and blossom blight of stone fruit and pome fruit trees worldwide. It has a more restricted distribution than the other species, occurring in Europe and Asia, but not in North America. Reports of its occurrence in South America are likely to be errors in identification. Recent identification of a new species in Japan suggests that it may not be present there, as previously thought, and reports from other parts of eastern Asia may have to be re-examined. It is a quarantine pest for Canada, the USA, Australia and New Zealand. One unusual introduction to the USA was resolved by eradication (Batra, 1979; Ogawa and English, 1991). Introduction could occur through the importation of infected fruit as well as of tree material for propagation and breeding, from which it could spread readily by means of conidia carried by the wind or insects.
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Ascomycota
- Subphylum: Pezizomycotina
- Class: Leotiomycetes
- Subclass: Leotiomycetidae
- Order: Helotiales
- Family: Sclerotiniaceae
- Genus: Monilinia
- Species: Monilinia fructigena
Notes on Taxonomy and NomenclatureTop of page
Persoon first used the specific epithet 'fructigena' in 1796 in assigning the name Torulafructigena to the conidial form of a brown rot fungus that he observed in Europe. However, Harrison (1933) concluded that “it is impossible with certainty to allocate Persoon's description to any of the present day species of Brown Rot Fungi”. In 1801, Persoon further described the conidial fungus under the name Monilia fructigena (Byrde and Willetts, 1977). Kunze and Schmidt later clearly described the same species as Oidium fructigenum, and in 1819, Schmidt included it in a descriptive collection of specimens of German fungi (Byrde and Willetts, 1977). Harrison (1933) studied the material of O. fructigenum and confirmed that it was Monilinia fructigena.
Aderhold and Ruhland (1905) were the first to describe the apothecia of this fungus, and also described the conidial state obtained from ascospore isolates. This description of the asexual form was similar to that for O. fructigenum by Kunze and Schmidt (1817). Sclerotinia fructigena as J. Schröt. ex Aderh. & Ruhland was the name then assigned to the teleomorph, but this is a later homonym of Sclerotinia fructigena (Pers.) J. Schröt. The correct current name is Monilinia fructigena Honey ex Whetzel. Following the establishment of the genus Monilinia by Honey (1928), his placement of the species in this genus (Honey, 1936) was validated by Whetzel (1945). For additional information on the nomenclature of this fungus, see Kohn (1979) and USDA/SMML (2005).
Holst-Jensen et al. (1997) have shown by examination of DNA sequences that the genus Monilinia is polyphyletic, with the two sections, Junctoriae and Disjunctoriae, clearly separate in origin. The section Junctoriae, which includes M. fructigena, also includes the type species Monilinia fructicola, and these species would remain in Monilinia if the sections were recognized as different genera.
Some level of intraspecific variation is observed in M. fructigena. Considerable variation in growth rate in culture has been observed between different Spanish isolates of the species (De Cal and Melgarejo, 1999). However, little intraspecific variation was found in the ITS region of ribosomal DNA in M. fructigena isolates from Denmark and Norway (Holst-Jensen et al., 1997) and France (Ioos and Frey, 2000). After intraspecific variation in the ITS region was observed between European and Japanese isolates (Fulton et al., 1999), morphological differences were described in culture, with the result that the Japanese fungus was proposed as a separate species (Van Leeuwen et al., 2002).
DescriptionTop of page
Apothecia cupulate, stipitate pale brown, margin entire, 3 mm diameter at maturity. Paraphyses unbranched, septate, 2-3 µm wide, not enlarged at apex.
Asci cylindrical, eight-spored, 160-180(-200) x 9-11 µm. Ascospores obliquely uniseriate or oblique, hyaline, eguttate, smooth, narrow-ellipsoid, ends tapered, but not pointed, 9-11(-13) x 5.0-6.6 µm.
Sporodochia scattered or confluent, buff to pale yellow-brown, 1-2 mm wide, up to 2 mm high. Conidia in branched chains, elongate-ellipsoid, limoniform or ovoid, hyaline, 15-25 x 12-16 µm. Arthric conidia sometimes present, 12-34 x 6-15 µm.
For a more detailed description, see Batra (1979; 1991).
Colony in culture colourless to white, margin entire, aerial mycelium initially sparse, later concentrically zonate. Sporogenous areas buff. Sclerotia present or absent, discoid to elongate, flattened: outer rind dark, three to four cells thick, cell walls thick, pigmented; medulla colourless, hyphae intertwined, 2-11 µm diameter, interhyphal spaces filled with gelatinous material.
For a more detailed description of the anamorph in culture, see Mordue (1979).
DistributionTop of page
M. fructigena is found throughout western and southern Europe and extends into the Scandinavian countries, eastern Europe, the former Soviet Union, the Middle East, India, and North Africa (CABI/EPPO, 2000; USDA/SMML, 2005). Recent identification of the common brown rot fungus in Japan, previously considered to be M. fructigena, as a separate anamorphic species, Monilia polystroma, may suggest reconsideration of other reports of M. fructigena from eastern Asia (Van Leeuwen et al., 2002). The new species has also been isolated in Hungary, within the known range of M. fructigena (Petróczy and Palkovics, 2009).
UK CAB International (1976) includes a record for presence in Brazil. EMBRAPA have since notified CABI that this record was a misidentification and that M. fructigena is not present in Brazil. Earlier reports of the species from Chile and Uruguay (UK CAB International, 1976) are also due to misidentification of other species of Monilinia (Malvárez et al., 2004; USDA/SMML, 2005).
In the USA, M. fructigena was reported from a pear [Pyrus communis] orchard in Maryland (Batra, 1979), but this minor outbreak was eradicated (Batra and Harada, 1986; Ogawa and English, 1991). It has also been erroneously reported from Florida (Florida Department of Agriculture and Consumer Services, USA, correspondence, 2000).
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: 12 May 2022
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|-Jammu and Kashmir||Present|
|Japan||Present||probably a different species (Van Leeuwen et al., 2002)|
|-Russian Far East||Present|
|Serbia and Montenegro||Present|
|United Kingdom||Present, Widespread||Introduced||Invasive|
|United States||Absent, Formerly present|
|-Florida||Absent, Invalid presence record(s)|
|Brazil||Absent, Formerly present|
|Chile||Absent, Formerly present|
|Uruguay||Absent, Formerly present|
IntroductionsTop of page
Risk of IntroductionTop of page
Brown rot is a serious disease causing significant losses on fruit crops. M.fructigena is a less serious pathogen than Monilinia laxa or Monilinia fructicola, and controls for brown rot are already in practice in the fruit growing regions. However, most countries quarantine for this pathogen. The most likely means of introduction of M. fructigena would be infected fruit brought in commercially or by individuals from other continents, but trees or scions with twig blight infections, unless quarantined, could carry the fungus more directly to populations of hosts.
Habitat ListTop of page
|Terrestrial||Managed||Cultivated / agricultural land||Present, no further details||Harmful (pest or invasive)|
|Terrestrial||Managed||Managed forests, plantations and orchards||Present, no further details||Harmful (pest or invasive)|
|Terrestrial||Natural / Semi-natural||Natural forests||Present, no further details||Natural|
Hosts/Species AffectedTop of page
Under suitable environmental conditions, M. fructigena will infect not only all cultivated drupaceous and pomaceous species, but also many other members of the Rosaceae. The extensive cultivation of fruit trees in temperate regions and their long lifespan ensure that hosts are readily available. The main commercial crops that are hosts to M.fructigena include apple [Malus domestica], pear [Pyrus communis], quince [Cydonia oblonga], plum [Prunus domestica], and sweet cherry [Prunus]. Sour cherry [Prunus] is a less important host than peach [Prunus persica], nectarine [Prunus persica], and apricot [Prunus armeniaca]. There are many records of the brown rot fungi attacking other plants (Byrde and Willetts, 1977; Tzavella-Klonari, 1985; Sharma and Kaul, 1989a; Faivre-Amiot and Geoffrion, 1996). Wild hosts may be sources of inoculum if located near orchards (Zehr, 1982).
Host Plants and Other Plants AffectedTop of page
Growth StagesTop of page
SymptomsTop of page
Blossom blight develops in the spring, particularly in moderately warm, moist weather. Infections occur on stamens, stigmas, petals or sepals, generating brown lesions that spread to other parts of the flower, and through peduncles to other flowers in the cluster and into the twigs. Affected flowers wilt and collapse, and some fall to the ground. Others remain on the tree, and sporulation on the blighted blossoms under moist conditions provides inoculum for further spread (Byrde and Willetts, 1977).
Brown rot on ripening or mature fruit typically develops as a rapidly spreading, firm, brown decay. Infection of fruits can take place at any time during fruit development, but the disease is only severe in ripe or ripening fruits. Infections of fruitlets during, or shortly after, flowering may result in quiescent infections on green fruit that become active before or after harvest. The first symptoms on ripe fruits are small, superficial, circular brown spots that quickly begin rotting (Byrde and Willetts, 1977). Conidial pustules usually develop on the infected areas under moist conditions. Within several days the fruits are completely rotten and almost the entire surface is covered with conidial tufts or vegetative mycelium. The cream-white to buff sporulating area may have concentric zones of sporulation produced in response to diurnal cycles. When the relative humidity is low and/or when the fruits are not ripe, no mycelium and very few or no conidial tufts develop (Byrde and Willetts, 1977). Eventually the whole fruit becomes discoloured and water is lost so that a mummified fruit is formed. The fungus often spreads by growth from diseased fruit to healthy ones in the same cluster or as conidia to other tissues (Xu et al., 2001b). Diseased fruits tend to remain attached to the tree as shoot dieback prevents formation of an abscission layer between fruit and peduncle. Mummified fruit hangs on branches of trees until spring or falls to the ground, where it remains throughout the winter months and becomes partly or completely buried beneath the soil or leaf litter (Byrde and Willetts, 1977).
Cankers usually develop from blighted twigs or branches by growth of mycelium into larger limbs of the tree (Byrde and Willets, 1977). An elliptical or spindle-fusoid canker forms with substantial gum production at the advancing margin. At times, the cankered area may girdle the twig and blight the portion distal to it. Leaves of infected twigs turn dark brown and remain attached instead of abscising. Usually cankers are restricted to twigs and do not extend into the previous year's wood. Cankers do not continue to enlarge from one season to the next. If the branch is not girdled, surrounding healthy tissue will produce calluses. When diseased twigs are not removed and environmental conditions are suitable for sporulation, active cankers produce conidia. In pear [Pyrus communis], twig blight occurs mostly through growth of the pathogen into the stem following blossom infection. Other more aggressive canker-causing fungi may colonize cankers and dead shoots.
Symptoms can vary on different crops. On apple [Malus domestica], fruit rot is very common and destructive; sometimes the fungus spreads into branches from the fruit and gives rise to cankers. A symptom referred to as 'black apple' may also develop. The colour of the rot is initially brown, but becomes jet black as the rot progresses (Byrde and Willetts, 1977). The skin of the apple then has a shiny smooth surface unruptured by conidiophores, and shrinkage of the apple tissue is insignificant until late in black apple development. This condition is mostly found in stored fruits. Fruit rot is common in pear and plum [Prunus domestica] as well, but less severe in peach [Prunus persica], nectarine [Prunus persica] and apricot [Prunus armeniaca].
List of Symptoms/SignsTop of page
|Fruit / extensive mould|
|Fruit / lesions: black or brown|
|Fruit / mummification|
|Growing point / dead heart|
|Growing point / dieback|
|Inflorescence / blight; necrosis|
|Leaves / wilting|
|Leaves / yellowed or dead|
|Stems / canker on woody stem|
|Stems / dieback|
|Stems / gummosis or resinosis|
|Stems / internal discoloration|
|Stems / necrosis|
Biology and EcologyTop of page
The conidia of M. fructigena are “dry air” spores (Hirst, 1953) that are not actively discharged, but are set free by air currents and wind. Although short and unspecialized, the conidiophores elevate the spore chains above the infected tissues and thus provide better exposure to air currents. Except when mummified fruit have fallen to the ground, infected fruits and peduncles are in positions on the tree that are suitable for efficient take-off and aerial dispersal of spores (Byrde and Willetts, 1977). The conidia of M. fructigena are disseminated by wind when temperatures are high, when relative humidities are low, and often at high UV light intensities. Rain splashes are important as a means of liberating spores. Apart from providing a method for dislodging conidia, rain droplets supply the moisture for germination and subsequent mycelial development. Shock waves produced ahead of the drops will also lead to the liberation of dry spores (Jarvis, 1962). Aerial dispersal results in the spread of spores over a wide area, whereas water splash dispersal brings about only short-range dissemination, mainly to other parts of the same tree or, in some instances, between adjacent trees. Roberts and Dunegan (1932) considered that transport by air was the most important way that spores of M.fructigena reach their hosts, but transport by water escapes the extreme environmental conditions to which wind-borne inocula are often subjected.
Animals are important vectors of this fungus, either incidentally or because of complex adaptations (Lack, 1989). Almost any insect attracted to rotting flowers or fruit has the potential to pick up and carry spores from sporulating mycelium to healthy, susceptible tissues, but those that create new wounds provide the necessary sites of infection for M. fructigena (Xu and Robinson, 2000; Xu et al., 2001b; 2007). The most important animal vectors are birds, wasps (Vespula spp.), beetles, especially the nitidulid beetles (Carpophilus spp.), flies (Diptera) including Drosophila spp., and Lepidoptera (Byrde and Willetts, 1977).
The brown rot fungi overwinter mainly in or on diseased mummified fruit either attached to the tree or on the ground. Other infected tissues on trees, such as twigs, peduncles and cankers on twigs or branches, can also serve as sources of primary inoculum. In the spring or early summer, when temperatures, day-length and relative humidities are suitable, tufts of conidiophores form sporodochia on the surface of the mummified fruit and infected tissues, and bear chains of conidia. Conidia are transported by wind, water or insects to young fruit. Initial infection is via wounds (Rekhviashvili, 1975; Xu and Robinson, 2000; Xu et al., 2001b; 2007), often scab lesions or sites of insect damage. Subsequent spread by contact between adjacent fruit is a minor cause of infection (Xu and Robinson 2000; Holb and Scherm, 2008). Growth cracks may also be infection courts on apple (Xu and Robinson, 2000; Holb and Scherm, 2008). Free moisture on the plant surface is not essential for the rapid germination and infection by conidia (Xu and Robinson, 2000).
Any infected tissue in which the moisture content is sufficient for sporulation may serve as a source of secondary inoculum. After the initial penetration of fruits, there is active mycelial growth, and the hyphae in the outer tissues of the fruit become closely interwoven to form a stroma. This has an outer rind, a medulla containing both hyphae and host cells, and an inner rind. The tissues in the centre of the fruit rot away leaving a hollow sclerotial sphere of leathery or rubbery consistency usually enclosing the seed or unrotted core of the fruit (Byrde and Willetts, 1977). Fruits may become infected at harvest time and then fruit rots can develop during the postharvest period. The fungus can survive long periods of adverse environmental conditions as mycelium within mummified fruits, twigs, cankers and other infected tissues. When conditions become favourable (usually after a dormant period), spores are produced on infected tissues and the fungus is dispersed to start a new cycle of infection, which coincides with early spring growth of host plants.
There are only a few records of the development of the sexual form of M. fructigena (Ibragimov and Abbasov, 1976; Batra, 1979; Batra and Harada, 1986). Apothecia may be produced in spring on mummified fruit that have overwintered on the ground. Mummified fruits that remain on the tree do not produce apothecia (Byrde and Willetts, 1977). Batra (1991) described apothecia observed from an unusual introduction to North America. The apothecia described in Japan (Batra and Harada, 1986), although not obviously different, may be the sexual state of the Japanese anamorphic species, Monilia polystroma.
The liberation of ascospores normally coincides with the emergence of young shoots and blossoms of plants (Ogawa and English, 1991). When spores alight on susceptible tissues under favourable environmental conditions, they germinate to initiate infections. In addition to the conidium and ascospore, a third type of spore is produced. This spore is known as a microconidium because of its small size. Unlike the conidium (macroconidium) and the ascospore, the microconidia do not function in propagation and dispersal, but rather as spermatia in mating. Microconidia are produced in abundance within small cavities and on the surfaces of mummified fruit (Byrde and Willetts, 1977).
M. fructigena is a pathogen of moist conditions, favoured by rain, fog and other factors that increase humidity, especially at the beginning of the host growth period; brown rot is rare in arid climates. Conidia are generally formed on mummified fruit and blighted twigs at temperatures of >5°C. Germination and germ tube growth are partially inhibited by light, but sporulation is enhanced. Conidia provide the inocula for most primary infections. Xu et al. (2001a) found 97% RH and temperatures of 3-25°C optimum for germination of conidia in the UK.
At harvest, apparently healthy fruit usually can be contaminated with spores, and decay may occur during storage and marketing. In latent infections the early infection of fruit does not produce symptoms of disease, and further differentiation of the fungus cannot take place until the fruit begins to ripen (Byrde and Willets, 1977). Mycelium generally have a greater potential than spores for causing infection in storage because they have greater reserves of food material at their disposal.
ClimateTop of page
|Cf - Warm temperate climate, wet all year||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year|
|Cs - Warm temperate climate with dry summer||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
|Dw - Continental climate with dry winter||Tolerated||Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)|
Notes on Natural EnemiesTop of page
Corke et al. (1975) found a trend towards reduced infection of fruit by M. fructigena on container-grown plum [Prunus domestica] trees experimentally inoculated in the trunk with the fungus, Trichodermaviride. Harada (1998) reported that the mycoparasite Lambertella corni-maris occurs on stroma of M. fructigena on apple fruits [Malus domestica]. Acid production by the host fungus is reported to stimulate production of antibiotic lambertellols by L. corni-maris (Murakami et al., 2007).
Means of Movement and DispersalTop of page
Conidia of the Monilia anamorph are dispersed by wind and rain-splash, and, where apothecia are formed, ascospores will be wind-disseminated (Batra, 1991).
Various types of insects, including wasps, beetles, flies and butterflies have been identified as vectors of Monilinia species (Byrde and Willetts, 1977). According to Lack (1989), any insect that visits both infected and uninfected fruit could serve as a vector; he specifically observed bees, wasps, fruit flies and syrphid flies on apple [Malus domestica] fruit infected with M. fructigena. Birds may also be vectors (Byrde and Willetts, 1977). Holb and Scherm (2008) and Xu et al. (2001b) report birds as wound agents in fruit orchards affected by M. fructigena.
The Australian phytosanitary authority has intercepted infected fruit (Mackie et al., 2005), as has occurred in the USA (USDA/SMML, 2005). The probable source of M. fructigena found on pear [Pyrus communis] trees at Beltsville, Maryland, USA, was not identified by Batra (1979), but only one variety growing at the experimental orchard at the agricultural station was infected.
Seedborne AspectsTop of page
The fungus could certainly infect seed or pits in rotted fruit, but fruit trees are not generally propagated by seed, and seedling infection is unlikely. Nevertheless, Richardson (1990) has reported seedborne Monilinia laxa on Corylus (hazelnut), which is also a host for M. fructigena (Mordue, 1979a: Tzavella-Klonari, 1985).
Pathway CausesTop of page
Pathway VectorsTop of page
|Host and vector organisms||Yes||Byrde and Willetts (1977); Lack (1989)|
|Plants or parts of plants||Yes||Batra (1991); Byrde and Willetts (1977)|
|Water||rain-splash carries ascospores and conidia||Yes||Batra (1991); Byrde and Willetts (1977)|
|Wind||ascospores and conidia||Yes||Batra (1991); Byrde and Willetts (1977)|
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 not visible to the naked eye but usually visible under light microscope|
|Fruits (inc. pods)||fungi/hyphae; fungi/spores||Yes||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Leaves||fungi/hyphae; fungi/spores||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Stems (above ground)/Shoots/Trunks/Branches||fungi/hyphae; fungi/spores||Yes||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Plant parts not known to carry the pest in trade/transport|
|True seeds (inc. grain)|
Impact SummaryTop of page
Economic ImpactTop of page
Although M. fructigena causes significant losses both before and after harvest, it is not easy to assess the overall losses it causes in a country or on a worldwide scale (Batra, 1991). Losses are highly visible to the grower, but are rarely worth the implementation of specific control measures in their own right. Early-maturing cultivars are most affected, but the majority of diseased fruits are those that would in any case be rejected for other reasons such as bruising or bird and insect damage (Smith et al., 1992). M. fructigena is less damaging than Monilinia fructicola or Monilinia laxa, although it occasionally causes economically important losses of apple [Malus domestica] and plum [Prunus domestica] fruits in Europe, particularly in hot and humid summers (Smith et al., 1992).
In 1972, Burchill and Edney reported 35.8% fruit infection in an English apple orchard. Ciferri reported 7.3% infection of apples in Italy. Preece reported mean losses of 0.2-1.5% in samples of Cox’s Orange Pippin apples taken from refrigerated stores in England between 1961 and 1965, with a range of 0.1-4.5% for individual orchards. In a survey carried out in a typical English commercial store, Evans stated that brown rot and other rots due to Botrytis cinerea and Penicillium spp. usually accounted for less than 5% loss in storage. See Byrde and Willetts (1977) for further details of these references.
According to Berrie (1993), average commercial losses due to fungal rots in apples have been maintained at <2% under UK conditions by the routine use of postharvest fungicide dips or drenches. In surveys of markets, stores and canning centres in Himachal Pradesh, India, the cumulative incidence of brown rot in harvested apples was 5.0-15.2%; the occurrence of M. fructigena varied from 2.1 to 14.2% (mean 6.72%), being more frequent under low-temperature conditions (Sharma and Kaul, 1989c). In central Europe, pre-harvest losses of apples due to brown rot are usually less than 10%, but losses of up to 46% have been reported (Holb and Scherm, 2007).
Risk and Impact FactorsTop of page
- Invasive in its native range
- Proved invasive outside its native range
- Has a broad native range
- Abundant in its native range
- Highly mobile locally
- Fast growing
- Has high reproductive potential
- Reproduces asexually
- Host damage
- Negatively impacts agriculture
- Negatively impacts livelihoods
- Reduced amenity values
- Highly likely to be transported internationally accidentally
- Difficult to identify/detect as a commodity contaminant
- Difficult to identify/detect in the field
- Difficult/costly to control
DiagnosisTop of page
Identification of Monilinia spp. has generally been based on cultural and morphological characters. The main distinguishing characters between species are: the colour and appearance of the conidial pustules, cultural characteristics of colonies, the host range, and the parts of the plant that are infected (Byrde and Willetts, 1977; Willetts et al., 1977; De Cal and Melgarejo, 1999; Lane, 2002). A commercial ELISA kit is available to identify Monilinia fructicola, but not M. fructigena or Monilinia laxa (Hughes et al., 1998; Gell et al., 2007).
In culture, M. fructigena has entire colony margins, a different conidia colour and longer conidium germ tubes than M. laxa (Penrose et al., 1976; Mordue, 1979a,b). M. fructicola produces more abundant conidia, stromata and microconidia, and has slightly smaller conidia than M.fructigena (Mordue, 1979a,c). M. fructicola is distinguished from M. laxa in having entire colony margins, by the colour of conidia, by the absence of hyphal anastomoses between germinating conidia, and in having longer conidial germ tube extension before branching (Penrose et al., 1976; Mordue, 1979b,c). These characteristics assist in the identification of typical cultures of Monilinia spp., but problems arise with atypical cultures. Differences have been observed among isolates of the same species (Byrde and Willetts, 1977; Harada, 1977; Batra, 1979; Wilcox, 1989; De Cal and Melgarejo, 1999). This variability is especially important when quarantine measures apply to one species, but not to another.
De Cal and Melgarejo (1999) have demonstrated that distance from the conidium to the first germ tube branch and growth rate under a long-wave UV/dark cycle provides a satisfactory method for differentiating species. M. laxa isolates can be easily distinguished from M. fructigena and M. fructicola on distilled water agar (2% agar, Oxoid) by the characteristic short-distance germ tube elongation, less than 60 µm, from the conidium to the first germ tube branch. M. fructigena and M. fructicola both produce germ tubes that grow for at least 220 mm before branching. These two species can then be differentiated from each other in culture under long-wave UV/dark conditions. Maximum growth rate (difference between diameters at days 5 and 3 after inoculation) of M.fructigena was 8 mm, whereas maximum growth rate of M. fructicola was 20 mm. Using different isolates, Van Leeuwen and Van Kesteren (1998) found that the combination of growth on potato dextrose agar (PDA) at 22°C under 12 h light (near-UV): 12 h dark, and length of the germ tube after 18 h incubation is sufficient to differentiate the fungi. Increase in colony diameter from day 3 to day 5 is the highest in M. fructicola, and the germ tubes are the shortest in M. laxa. The synoptic key produced by Lane (2002) relies on seven “critical characters” of colonies in culture for 10 days, including rate of growth under 12 h near-UV: 12 h dark, although growth alone could not be used to separate species due to intraspecific variation. Colony colour on 4% PDA was still useful in distinguishing M. fructigena from the other two species.
Efforts continue to develop a more rapid, simple and objective method of diagnosis that addresses all species. A number of physiological or chemical features separate the three related Monilinia spp: M. fructigena is unable to produce large numbers of conidia in PDA in the dark without the addition of indolyl-3 acetic (Wiltshire, 1920; Kahn, 1966), isoelectric patterns of the extracellular enzymes a-L-arabinofuranosidase and pectinlyase are useful for confirming morphological identifications (Willetts et al., 1977), and a monoclonal antibody-based immunoassay was developed to identify M.fructicola and has been tested with some isolates of Monilinia from an EU collection (Hughes et al., 1998). A 418-bp group-I intron has been located in the small subunit (SSU) rDNA gene of M. fructicola that is absent from the other two species (Fulton and Brown, 1997). Consequently, PCR primers specific to the 3´-region of the intron together with the SSU rDNA primer NS5 enabled amplification of a 444-bp product only from M. fructicola and fruit tissue infected with it. This allows for the rapid and sensitive detection of this invasive species for Europe.
Ioos and Frey (2000) found low interspecific polymorphism in the ITS region of the three Monilinia species, but developed primers permitting identification to species in naturally infected fruit. Also observing a high level of similarity in the ITS region of rDNA among the species, Gell et al. (2007) developed a different PCR protocol using four sets of primers, three of them not related to the ITS region, for identification of the three major Monilinia species in plant material. Côté et al. (2004) reported a multiplex PCR method for distinguishing among four species causing brown rot, including the recently identified Monilia polystroma, in naturally infected fruit. Random Amplified Polymorphic DNA (RAPD) analysis was used to identify a PCR product exhibiting clear differences among the four species, and PCR primers were designed to detect the polymorphisms.
Detection and InspectionTop of page
Disease symptoms are clearly visible in the field and in storage (see Symptoms).
To distinguish M. fructigena from the other two brown rot fungi, the fruit with lesions should be incubated to obtain sporulation or/and the fungus isolated on suitable media to observe cultural characteristics. Molecular tests may be done on mycelium from pure culture or on infected fruit (see Diagnosis).
Similarities to Other Species/ConditionsTop of page
The brown rot fungi on species of Rosaceae are all virulent pathogens with similar life cycles and biology, producing the same types of symptoms on blossoms, leaves and fruits (Byrne and Willetts, 1977). Therefore, it is difficult to differentiate M. fructigena from the other two widespread brown rot fungi, Monilinia fructicola and Monilinia laxa, by its morphological characteristics (Batra, 1979) or by symptoms on hosts. Major distinctions from M. laxa include the presence of entire colony margins, buff conidium colour, and long conidium germ tubes (Mordue, 1979a,b). Features distinguishing the species from M. fructicola in culture include generally fewer conidia, stromata and microconidia in M. fructigena, and slightly larger conidia with a different colour in mass (Mordue, 1979a,c). M. fructigena grows more slowly than M. fructicola on potato dextrose agar (PDA) medium under long-wave UV light (De Cal and Melgarejo, 1999). Light is essential for sporulation in M. fructigena, but not in the other two species (Sharma and Kaul, 1989b). Byrde and Willetts (1977) provide a table of contrasted characters of the brown rot fungi, and Lane (2002) has produced a synoptic key to these three species in culture, based on examination of representative isolates.
In Japan, the brown rot fungus previously considered to be M. fructigena has been identified as a separate anamorphic species, Monilia polystroma, differing in cultural characters (Van Leeuwen et al., 2002) as well as the sequence of the ITS region of rDNA (Fulton et al., 1999). The Japanese isolates produced more stromata on cherry agar, had a significantly higher mean growth rate on PDA, and produced generally smaller conidia on both cherry agar and inoculated pear fruit [Pyrus communis].
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.
M. fructigena has been intercepted by phytosanitary authorities in Australia (Mackie et al., 2005), New Zealand (Byrde and Willetts, 1977) and North America (USDA/SMML, 2005). The species is a Regulated Pest for both Canada (CFIA, 2009) and the USA (USDA/APHIS, 2009), and a “notifiable” pest in New Zealand (Biosecurity New Zealand, 2006). The government of Australia has developed a protocol for its diagnosis to assist in preventing entry into that country (DAFF, 2008).
A key for identification of the major Monilinia species causing brown rot was published by EPPO (Lane, 2002) and molecular methods for rapid diagnosis in infected fruit have been developed (Ioos and Frey, 2000; Côté et al., 2004; Gell et al., 2007).
Losses due to M. fructigena are rarely worth specific control measures in their own right. Apart from avoidance of very susceptible cultivars in disease-prone districts, few control measures are specifically aimed at this fungus. By reducing the amount of inoculum produced, fungicides used for the routine control of foliar diseases provide an element of incidental control that, in practice, is often sufficient. Prospects for resistance breeding are limited, at least in apple [Malus domestica], because most resistant cultivars are of the cider type with fruit unsuitable for dessert use. However, much research has been done in Europe in breeding for resistance, particularly in eastern Europe.
Protective fungicidal treatments provide the best control for fruit rot. The proper use of fungicides with some systemic activity protects fruit, reduces the amount of sporulation formed on the infected tissue, and reduces sources of overwintering inoculum. There is an extensive range of fungicides available for brown rot control, including the dicarboximides (iprodione and vinclozolin), benzimidazoles (benomyl and thiophanate-methyl), triforine, chlorothalonil, ergosterol biosynthesis inhibitors (myclobutanil, fenbuconazole, and propiconazole), and anilinopyrimidines (Zhang et al., 1991; Vucinic, 1994; Reynaud, 1997; Rueegg et al., 1997; Cotroneo et al., 1998). Other fungicides used are copper compounds, sulphur, and captan (Byrde and Willetts, 1977). The new fungicides, pyraclostrobin and boscalid, are effective against M. fructigena and Monilinia laxa (Spiegel and Stammler, 2006). The selection of a fungicide or mixture of compounds is often influenced by the need to control other diseases that may occur more or less simultaneously with brown rot, such as scab, powdery mildew, rust, russet scab, or grey mould. Insect control may be an important consideration because M. fructigena must infect primarily through wounds (Xu and Robinson, 2000; Holb and Scherm, 2008).
Fungicide resistance in M. laxa and Monilinia fructicola has become evident following multiple applications of dicarboximides and benzimidazoles in several parts of the world (Gilpatrick, 1982; Ogawa et al., 1984). However, evidence of resistance to these fungicides in M. fructigena has not been reported in the field. To prevent selection of fungicide-resistant strains, it may be better to combine fungicides having different modes of action (Ogawa et al., 1975; Zehr, 1982).
Cultural Control and Sanitary Methods
The intelligent location of orchards can reduce the likelihood of severe outbreaks of disease. Limited benefit may also follow from measures designed to alter the environment in established orchards in the host's favour, e.g. pruning for increased air circulation (Byrde and Willetts, 1977). Cultural practices such as the removal of mummified fruit and pruning of infected twigs, with subsequent burning or deep-burying, and the removal of wild host plants near orchards, reduce the inoculum level, but these procedures alone are not sufficient to control the disease (Zehr, 1982). Nevertheless, Holb and Scherm (2007) found that fallen or thinned immature fruit infected with M. fructigena on the ground provided a significant source of inoculum in Hungarian apple orchards. Labour-intensive removal of such fruit could be economically feasible for organic management operations where chemicals used for disease control chemicals were less effective. Wormald (1954) emphasized that hygiene is equally necessary during and after seasons of light infection. Good hygiene can also reduce the population of insects that serve as spore vectors.
Manuring can have some influence on disease incidence and applications of potassium have brought about a reduction in disease incidence on apricots [Prunus armeniaca] (Vasudeva, 1930; Byrde and Willetts, 1977). High doses of nitrogen fertilizer are positively correlated with infection by M. fructigena (Daane et al., 1996).
Injuries to the plant may result from weather conditions. Hail can readily damage fruit, and it is useful to apply a protectant fungicide without delay when such injury occurs (Byrde and Willetts, 1977). Care during picking and handling is essential, and fruit should be picked with its stalk intact (Wormald, 1954). Particular care is needed in packing and storage of fruit because the fungus can grow from one fruit to others in contact with it. Damaged fruit should not be stored (Wormald, 1954). Mechanical harvesting of peaches [Prunus persica] can also cause injuries that may lead to severe rotting.
Control of Vectors
Control of insects that serve as vectors and/or provide wounds for infection, is essential for effective control of M. fructigena. Fungicides do not control infection if applied after mechanical injuries have become inoculated. Bird feeding may be reduced in orchards remote from houses by the use of explosive scares; wasp nests can be sought out and destroyed. Direct control of other vectors that are often attracted to rotten and damaged fruit seems difficult to achieve (Byrde and Willetts, 1977). However, Holb and Scherm (2007) attributed lower level of brown rot in orchards under integrated management in part to control of wound-creating insects through the use of insecticides that are not part of organic management. Forecasting for insect control, particularly of codling moth (Cydia pomonella), in organic management is needed to prevent injuries that are major infection courts for M. fructigena (Holb and Scherm, 2008).
Once the fruit is picked, alteration of the environment to the selective disadvantage of the pathogen is easily achieved. When fruit is chilled to below about 5°C in transit and storage, the growth of the fungus is very slow. Hydro-cooling, or hydrair-cooling, is now extensively used on peaches to prevent rot after harvest in the southeastern USA, but it is generally necessary to add fungicide to the chilled water (McClure, 1958; Wells and Bennet, 1975; 1976), or to have already treated the fruit in a non-emulsifiable wax formulation of a fungicide (Bennet and Wells, 1976). Gamma irradiation of apples reduces rot caused by M. fructigena (Janitor and Paulech, 1978; Tiryaki et al., 1994; Marcadi et al., 1998). A combination of hot water and fungicides also controls M. fructigena rot of apples (Sharma and Kaul, 1990).
Non-fungicidal postharvest treatments under investigation involve the use of materials that induce resistance, such as calcium treatments or surface coatings (Bancroft, 1995). The search for natural anti-microbial substances of metabolic origin is also promising. Of these compounds, the hydrolytic reaction products from glucosinolates are good candidates due to both their anti-microbial action and their tolerance by the plants; the isothiocyanates are generally active for in vitro and in vivo control of M. laxa (Mari et al., 1993; 1996), but have not been tested against M. fructigena. They are found in a number of edible plants, particularly the Brassicaceae.
Many factors have been implicated in host resistance to M. fructigena, but the genetic basis of resistance is poorly understood. Breeding for M. fructigena resistance is a major objective in Europe (Barsukova and Tuz, 1985; Grigortsevich, 1985; Nitransky, 1986; Barsukova and Gryuner, 1986; Grigorov, 1987; Bozhkova, 1995; Cantoni et al., 1996; Paunovic et al., 1996). In practice, many cultivars of fruit trees have been proved resistant (Rekhviashvili, 1973; Vasilev, 1975; Byrde and Willetts, 1977; Iliev and Shchrkova, 1979; Angelov, 1980; Iliev et al., 1986; Nitransky, 1986; Sharma and Kaul, 1988; Cimanowski and Pietrzak, 1991). Difficulty occurs with incorporation of factors from resistant varieties due to customer preferences with respect to apple and pear [Pyrus communis] fruit (Byrne and Willetts (1977).
Few attempts have been made in the biological control of M. fructigena; some of them are described by Byrde and Willetts (1977), including experiments with Trichoderma viride, which has not been prepared for commercial application. Some experimental applications of the bacteria Bacillus subtilis and Pseudomonas cepacia in strawberries [Fragaria ananassa] and sweet cherries [Prunus] have been made (Marquenie et al., 1999). Falconi and Mendgen (1994) showed that isolates of Aureobasidium pullulans, Epicoccum purpurascens [Epicoccum nigrum], Sordaria fimicola, and Trichoderma polysporum, applied individually or in mixtures to wounded apples, gave good protection from M. fructigena. Some experiments have been undertaken in commercial orchards involving control of twig blight and fruit rot of peaches and plums [Prunus domestica] due to M. laxa by the application of fungal antagonists such as E. nigrum, Penicillium frequentans [Penicillium glabrum], or Penicillium purpurogenum (De Cal et al., 1988; 1990; Madrigal et al., 1994; Larena and Melgarejo, 1996; Pascual et al., 1996; 1998; Melgarejo et al., 1998) or the control of fruit rot of peaches induced by M. fructicola using Bacillus subtilis (Pusey and Wilson, 1984; Pusey et al., 1988). These antagonists may also be effective against M. fructigena. Formulations of P. frequentans were found more effective than a fungicide in reducing conidial numbers of Monilinia spp. (primarily M. laxa) on peaches in the orchard in Spain (Guijarro et al., 2007). Four applications of E. nigrum conidia in the season significantly reduced post-harvest brown rot in most of a set of trials controlled in Italy, France and Spain (Larena et al., 2006), but the greatest effect for stone fruit was found at the time of pit hardening and in the month before harvest (De Cal and Melgarejo, 2009).
Integration of the various means of control of brown rot in order to reduce costs and damage to the environment due to the application of fungicides and insecticides can be achieved, but requires considerable study of the variables of the host crop, environmental factors and interactions between the fungus, its vectors, and biological control agents. As Zehr (1982) notes, the need to control other fungal pathogens of the particular host in a certain location must also be considered in a chemical application programme for brown rot.
Older cultural and sanitary control methods were (and still can be) directed at removing sources of inoculum; chemical controls are directed at protecting the host from infection by inoculum regardless of its source. Therefore investigation of factors affecting the production and distribution of conidia is necessary for determination of effective and timely chemical use. Holb and Scherm (2007) found that rotting of dropped and thinned fruit provided a source of inoculum between early spring and the appearance of ripening apple fruit later in season. According to Holb (2008), disease incidence in apple orchards was significantly related to cumulative conidium numbers in air, which increased through the season, particularly after the first appearance of infected fruit. A diurnal periodicity was observed for conidium numbers, with peaks in the afternoon, corresponding to periods of higher temperatures and lower relative humidity. In the UK, Xu et al. (2001a) determined that conditions of temperature and relative humidity are not limiting for sporulation or spore germination.
Bannon et al. (2009) also observed a diurnal pattern of spore concentrations of M. fructigena in the air, with an increase occurring with higher temperature that can be related to the development of the fungus. Wind effects on inoculum density in the air appeared to be related to the local physical and topological conditions in the orchard.
Gaps in Knowledge/Research NeedsTop of page
The identity of the Monilinia species reported as M. fructigena in eastern Asia, and possibly also western Asia, should be clarified using molecular methods.
ReferencesTop of page
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Villarino M, Melgarejo P, Cal A de, 2016. Growth and aggressiveness factors affecting Monilinia spp. survival peaches. International Journal of Food Microbiology. 6-12. DOI:10.1016/j.ijfoodmicro.2016.01.023
Volkova J, Vilka L, Stanke L, Rancane R, Bazenova A, 2013. Molecular characterization of Monilinia laxa and M. fructigena causing brown rot of sweet cherry in Zemgale Region of Latvia. Acta Biologica Universitatis Daugavpiliensis. 13 (1), 165-172.
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