Monilinia (brown rot of stone fruit)

Taxonomy

Domain	Eukarya
Kingdom	Fungi
Phylum	Ascomycota
Subphylum	Pezizomycotina
Class	Leotiomycetes
Subclass	Leotiomycetidae
Order	Helotiales
Family	Sclerotiniaceae
Genus	Monilinia

Scientific Name

Monilinia fructicola

Scientific Name Synonyms

Monilia fructicola

Sclerotinia fructicola

Common Name

brown rot

Authors:Elizabeth Bush and Keith Yoder, Virginia Tech

Reviewed by:Alan R. Biggs, West Virginia University

Pathogen

Brown rot is one of the most destructive diseases of stone fruits, such as peach, nectarine, apricot, cherry and plum. When environmental conditions favor this disease, crop loss can be devastating. Three species of Monilinia and the recently described anamorph, Monilia polystroma, formerly lumped into M. fructigena, cause brown rot in temperate regions on members of the Rosaceae. Monilinia fructicola colonizes blossoms, twigs and fruit, primarily on Prunus spp., but also on pome fruit or other Rosaceae. Monilinia laxa can colonize blossoms, twigs and fruit, but is generally considered more of a problem on blossoms and twigs. M. fructigena is primarily a problem on fruit of apple, pear and other pome fruits. Monilia polystroma is reported to cause rot on both pome and stone fruits.

Symptoms and Signs

Although brown rot damage is typically observed on fruit, the fungus may also infect blossoms, leaves, and shoots. Blighted blossoms turn brown and stick to shoots in a gummy matrix in which gray to tan fungal spore masses are produced.

Shoots infected by the brown rot fungus develop sunken, brown, elliptical cankers that may become gummy. Cankered areas are usually restricted to new shoots and typically occur as the disease advances from infected blossoms. Gray to tan fungal spore masses may be produced in cankered areas. If a shoot is girdled by a canker, the shoot will die and leaves will turn brown, but remain attached to the branch for a few weeks.

Symptoms on ripening peaches and nectarines may first appear as small, circular spots that enlarge or coalesce. On mature fruit, these lesions develop and enlarge rapidly. When environmental conditions favor disease development, ripe fruits may completely rot within two days. Tan to gray spore masses are often evident on rotting fruit. Diseased fruits typically shrivel and turn brown to black, either dropping to the ground or remaining attached to the tree. These tough, shriveled fruits, termed mummies, are a major source of overwintering fungal inoculum, but the brown rot pathogen can also overwinter in cankers and infected fruit pedicels.

Symptoms on immature sweet cherries may be small (3/16” to 3/4” diameter), red-haloed spots or sunken, necrotic spots, up to approximately 1/4” in diameter. Symptoms on mature cherries are similar to those on peach and nectarine. Fur-like clusters of gray to tan spore masses develop on plums colonized by the brown rot fungus.

Table 1. Summary of symptoms of three brown rot pathogen on pome and stone fruit (adapted from summary table by Byrde and Willetts, 1977).

Host	M. fructicola	M. laxa	M. fructigena
plum	Severe fruit rot, twig and blossom blight	Fruit rot, leaf and blossom blight, cankers	Fruit rot
cherry	Fruit rot, severe blossom blight	Fruit rot, blossom blight	Fruit rot just prior to ripening
peach and nectarine	Fruit rot, blossom, leaf and twig blight, cankers may be severe	Fruit rot, blossom and twig blight, cankers (sometimes severe)	Fruit rot (not typically severe)
apricot	Fruit rot, blossom and twig blight; severe cankers	Fruit rot, blossom and twig blight, cankers (sometimes severe)	Fruit rot (not typically severe)
apple	Fruit (not serious), occasional spur blight	Blossom blight, cankers	Fruit rot, cankers sometimes
pear	Fruit rot on injured or ripe fruit (rare)	Blossom blight on spurs (minor)	Fruit rot
quince	Fruit rot, twig blight	Fruit rot, blossom, leaf and twig blight	Fruit rot

Ecology and Spread

The brown rot fungus most commonly overwinters on fruit mummies on the tree and on the ground, in infested crop debris and in cankers. Sporulation of the fungus is favored by moderate temperatures (13 C to 25 C) and wet weather. Spread of the fungal spores to new infection sites occurs by wind and rain-splash. Insects, such as honey bees or beetles, may also transport the fungal inoculum to new infection sites.

Infections by the brown rot fungus may be initiated early in the growing season on blossoms and/or new shoots. Blossoms of stone fruit species differ in their susceptibility to this fungus, with apricot being the most susceptible, followed by sweet cherry, peach, sour cherry and plum. Blossom blight incidence is affected by both temperature and the length of time blossoms are wet. Blossom infection on peach and cherry can occur over a very broad range of temperatures (0 C to 30 C), but is optimum from 22 C to 25 C. However, when the weather is wet for 24 hours or more infection by the brown rot fungus is favored, regardless of the temperature.

Blossom blight is a concern even when outbreaks are not severe enough to significantly reduce the fruit crop directly. This is because fungal spores produced on blighted blossoms and on the resulting twig cankers can provide inoculum for infection of ripening fruit later in the growing season. The cankered shoots serve as a bridge in the disease cycle, allowing the brown rot fungus a means of survival during and between growing seasons, in addition to producing spores for future fruit infections. When cankers do not girdle and kill the shoot, the fungus can overwinter and produce spores in the canker for one to two years. Brown rot twig infection also makes twigs susceptible to additional disease problems by more destructive canker-causing organisms, such as the fungus Leucostoma.

Generally, stone fruits become more susceptible to brown rot as fruits ripen. Humid or wet conditions favor sporulation and infection by the brown rot fungus, so when these conditions are present during fruit ripening, serious brown rot outbreaks may occur. During favorable environmental conditions, large numbers of spores are produced on diseased fruits; these spread and infect ripening fruit. Fruits injured by oriental fruit moths, Japanese or green June beetles, other insects or hail are very susceptible to infection by the brown rot fungus. Harvested fruit is also commonly contaminated with spores of the brown rot fungus and this can result in infection during storage, especially if fruits were injured during harvest.

Green fruit are susceptible to infection prior to pit hardening. With peaches, nectarines, and plums, early infections may remain quiescent until the fruit ripening phase when they develop into visible rot symptoms. After pit hardening, green fruit are generally not susceptible to infection by the brown rot fungus. However, brown rot can occur on green fruit when they are:

• thinned after the pit hardens and left on the ground
• injured by insects, hail, birds, or by other means
• freeze-injured or stunted and remains on the tree

Brown rot on green fruit is a serious problem, because large amounts of fungal inoculum can be produced on diseased fruit. The inoculum produced may spread and infect ripening fruit.

The apothecium/ascospore is the sexual stage of the brown rot pathogens. This is observed rarely for some species (e.g. M. laxa and M. fructigena) and reported in some locations and not others. In some locations in the U.S. the sexual stage of M. fructicola is commonly reported, but not in others (e.g. Virginia). Apothecia are produced on fruit mummies on the ground, or mummies slightly buried under soil. The apothecia produce copious quantities of inoculum. Presence of apothecia under stone fruit trees is cause for serious concern and indicates that proper sanitation practices are not being followed.

Other sources of brown rot inoculum include early maturing stone fruit cultivars that may harbor inoculum for infections on later maturing fruit cultivars. For example, disease may progress and inoculum levels may increase on earlier ripening crops, such as cherries; this inoculum may then be available to infect later ripening crops, such as peaches, nectarines, and plums. This can also occur when inoculum produced on earlier ripening cultivars of the same fruit, such as peach, infects later ripening ones nearby. Also, ornamental flowering stone fruit species, such as ornamental plum or quince, and wild stone fruit species in the area, may provide inoculum for new infections on stone fruit trees. In any of the situations outlined above, when weather conditions are conducive to brown rot development and a progression of inoculum-production occurs, starting with the earliest ripening stone fruit and progressing to the latest ripening one(s) in an area, a brown rot epidemic is likely.

Geographic Distribution

Monilinia spp. occur throughout the world. Monilinia fructicola is widespread in North America, and also found in Australia, Asia, Africa, Central America and the Caribbean, South America, and New Zealand. M. fructicola has not been reported in Europe where it is currently classified as a quarantine pathogen. Monilinia laxa is present in Europe, South America, Asia, Australia, Africa and North America, where it has most commonly been reported in the Pacific Northwest, but has also been reported to have spread north and east. M. fructigena is widespread in Europe and parts of Asia. In the 1970s it was identified in Maryland, but subsequently eradicated. It has also been reported in parts of South America. The recently described Monilia polystroma (formerly lumped into M. fructigena) causes brown rot in Japan and has also been reported in Hungary, China, Czech Republic, Poland, Serbia and Switzerland.

Management

In regions with humid climates, adequate control of brown rot will typically require both cultural and chemical controls. Sanitation practices that reduce the amount of fungal inoculum are integral to brown rot control. It is important to remove as much infested plant material as possible to reduce overwintering fungal inoculum. Pruning practices that promote good air circulation and sunlight penetration into the tree canopy also can help to prevent conditions that favor infection and development of the brown rot pathogen.

• During the dormant season, remove all fruit mummies to reduce pre-bloom inoculum-production. This may be easier to do with peaches, which have large mummies, in contrast to cherries, which have smaller, less conspicuous mummies.
• Prune out weak or dead wood in the spring, taking care to remove any cankered shoots.
• Open up the tree canopy by careful pruning. This will increase sunlight penetration, which reduces the length of the wetting period in the canopy and improves fruit coloring. Open canopies also allow better fungicide coverage, which improves fungicide efficacy.
• When thinning fruit take note of the following precautions:

-Thin fruit so that mature fruits will not touch. Areas of contact between fruit provide ideal environments for disease and insect pests and favor prolonged wetting.

-Remove stunted fruit, which may be more susceptible to brown rot and will add little to fruit production.

-Peach or nectarine fruits that are thinned before the pit hardening stage of development can be left on the ground beneath the tree, since fruit at this stage will decompose rapidly and not serve as sporulation sites for the fungus.

-If peach or nectarine fruit is thinned after the pit hardens, remove thinned fruit from the site.

• Harvest fruit carefully and try to avoid injuries that predispose the fruit to brown rot during storage.
• Harvest all fruit so that they do not rot in situ and form overwintering pedicel infections and cankers.

Research in California associated excess nitrogen with increased susceptibility to brown rot, so follow recommended rates for nitrogen application and do not apply excess amounts.

Monitor stone fruit crops for symptoms of blossom blight a couple of weeks after bloom. If symptoms are evident, an earlier preventative fungicide spray program for brown rot will be warranted. Also monitor trees for insects that injure fruit, such as Japanese or June beetles, to determine if levels of insects or fruit injury warrant implementation of control tactics for insects. Also, check fruit for injury after hailstorms. Birds can also initiate wounds on ripening fruit, especially cherries, so some growers may need special tactics to prevent bird damage.

Most commercial stone fruit cultivars are susceptible to infection by the brown rot fungus if favorable conditions occur during the 3-week ripening period. During the stone fruit ripening period, weather conditions in some locations may vary much from year to year, so disease pressure may vary from year to year. Other factors that favor severe brown rot outbreaks, such as hailstorms or insect injury, also vary from year to year, causing a cultivar to appear resistant one year, but very susceptible the next. In general, nectarines are more susceptible than peaches and sweet cherries are more susceptible than tart cherries because of their tendency to crack as they swell during the pre-harvest period. Some of the cracking may be directly due to absorption of moisture from rain, which also favors spread and infection by spores of the brown rot fungus. The following peach cultivars have been reported to be less susceptible to brown rot: Elberta, Glohaven, and Babygold No. 5. Peach cultivars reported as highly susceptible are: Belle of Georgia, Coronet, Early East, Hale Harrison Brilliant, Halehaven, Maybelle, Mayflower, Raritan Rose, Redbird, Southhaven and Summercrest.

Fungicides must be applied before brown rot infection occurs. During the bloom period, preventative sprays to protect blossoms from infection should begin when pink begins to show in the flower buds. Preventative treatments during the three-week pre-harvest period are very important for fruit rot control. Repeat applications are typically required up to one week before harvest to protect fruit, depending primarily on the frequency and intensity of wet periods during the growing season.

Consult your local Extension office for fungicide product recommendations applicable to your state. Be aware that the brown rot fungus can develop resistance to several classes of fungicides, and avoid exclusive use of those products. Rotation or alternation of products from different classes of fungicides is the best approach.

Diagnostic procedures

The anamorphic stage of the fungus is typically useful for diagnostics. Monilinia spp. readily sporulate on affected plant tissue (e.g. blossoms, fruit), so identification to genus level is easily made by examination of conidia taken from tissue with a compound microscope. Moist chamber incubation may be necessary in some cases for spore production and alternating light/dark with near UV light promotes sporulation of this fungus. Brown rot fungi can be readily cultured on potato dextrose agar (PDA).

The hyaline, ellipsoid, ovoid /lemon-shaped, single-celled conidia are produced in chains in gray to light tan, cushion-shaped sporodochia on plant tissue. Microconidia (2.5 µM to 3 µm) may also be associated with M. fructicola; these are produced on bottle-shaped phialides on decayed fruit or in old cultures. Conidial width/length is not useful for separation of species, since there is overlap. Conidia also differ in size between winter and summer. The dimensions of conidia have been reported as 12-34 µM x 9-15 µM (M. fructigena), 8-23 µM x 7-16 µM/5-19 µM x 4-12 µM (M. laxa, summer/winter conidia) and 8-28 µM x 6-19 µM (M. fructicola).

Speciation of the brown rot pathogens has traditionally relied on one or more of the following: colony characteristics, growth rate and sporulation on potato dextrose agar (PDA); morphology of germ tubes and anastomosis; however, some of these characteristics are qualitative, may be subject to variability, and, therefore, are not completely reliable for confident identification to species. Lane (2002) developed a synoptic key for differentiation of M. fructicola, M. fructigena and M. laxa, which is based on cultural characteristics.

Colony characteristics of three brown rot pathogens on potato dextrose agar (commercial PDA, 39 g/liter) incubated under diurnal light/dark for 12 days at 22° C have been well-described by van Leeuwen and van Kesteren (2014) and some of their observations are summarized in Table 2. Colony characteristics of M. polystroma are reported to be similar to M. fructicola; however, M. polystroma produces black stromatal plates after 10 to 12 days of incubation.

Table 2.Colony characteristics of three brown rot pathogens on PDA incubated under diurnal light/dark for 12 days at 22° C (van Leeuwen and van Kesteren, 2014).

Pathogen	Pattern	Growth habit	Sporulation	Color of sporodochia
M. fructicola	Colony margin mostly even	Continuous radial growth	All over the surface of the colony	Grayish-yellow
M. laxa	Rosette pattern with dark rings between rosettes where growth cessation occurred	Radial growth periodically stops	Spores are produced tightly appressed to agar in new growth, but in older cultures (10 to 14 days) tufts of aerial mycelium develops where sporulation occurred	Grayish-yellow
M. fructigena*	Colony margin mostly even	Continuous radial growth	Aerial mycelium formed in concentric rings in which sporulation occurs	Cream/buff-yellowish
*some isolates produce rosette in dark

Van Leeuwen and van Kesteren (2014) also described growth rates of three brown rot pathogens (Table 3):

Table 3.Growth rates of three brown rot pathogens on PDA after 3 days under diurnal light at 22° C.

Pathogen	Colony diameter (mm)
M. fructicola	43.6 (31.0-53.0)
M. laxa	21.5 (17.0-30.0)
M. fructigena	21.1 (15.0-29.0)

The length of the germ tube and number of germ tubes per conidium was found to be a relatively reliable morphological characteristics to differentiate species by van Leeuwen and van Kesteren (2014); however, this method was not 100% reliable, and would not be very practical for the typical diagnostic laboratory.

A number of researchers have developed conventional or quantitative PCR methods to distinguish brown rot pathogens. Species specific primer sets (Hughes et al., 2000; Ioos and Frey, 2000; Cote et al., 2004) distinguish M. laxa, M. fructicola, and M. fructigena and were reported to not cross-react with M. polystroma by the EPPO (OEPP/EPPO, 2009). A conventional, multiplex PCR reaction developed by Cotes et al., 2004 produces amplicons from DNA extracted directly from brown rot-diseased fruit for all four brown rot pathogens (M. fructigena, M. fructicola, M. laxa, and M. polystroma) that differ adequately in size to distinguish by gel electrophoresis. The primer sets used by Cotes et al. (2004) were developed based on random amplified polymorphic DNA analysis since the ITS region of these four species is highly conserved. A quantitative PCR test, using Taqman probes, was developed by van Brouwershaven et al. (2009) and has been validated in Europe. However, this assay only distinguishes M. fructicola from the other three brown rot pathogens.

Resources and References

1. Byrde, R. J. W., and Willetts, H. J. 1977. The brown rot fungi of fruit: their biology and control. Pergamon Press, Oxford.
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4. Biggs, A. R., K. D. Hickey, and K. S. Yoder. 1995. Peach and nectarine brown rot. Edited by H. W. Hogmire, Mid-Atlantic Orchard Monitoring Guide. Ithaca, NY 14853-5701: Northeast Regional Agricultural Engineering Service, Cooperative Extension.
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9. Daane, K. M., R. S. Johnson, T. J. Michailides, C. H. Crisosto, J. W. Dlott, H. T. Ramirez, G. Y. Yokota, and D. P. Morgan. 1995. Excess nitrogen raises nectarine susceptibility to disease and insects. California Agriculture 49 (4):13-18.
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14. Leeuwen, G. C. M. v., and Wageningen, U. 2000. The brown rot fungi of fruit crops (‘’Monilinia’’ spp.), with special reference to ‘’Monilinia fructigena’’ (Aderh. & Ruhl.) honey. s.n, Wageningen.
15. Leeuwen, v. G. C. M. a. K., van H.A. 1998. Delineation of the three brown rot fungi of fruit crops (‘’Monilinia’’ spp.) on the basis of quantitative characteristics. Canadian Journal of Botany 76:2042-2050.
16. OEPP/EPPO. 2009. Monilinia fructicola. EPPO Bulletin 39:337-343.
17. Ogawa, J. M., E. I. Zehr, and A. R. Biggs. 1995. Compendium of stone fruit diseases. Edited by J. M. Ogawa, E. I. Zehr, G. W. Bird, D. F. Ritchie, K. Uriu and J. K. Uyemoto. St. Paul, MN 55121-2097: The American Phytopathological Society.
18. Peterson, D. Table of peach cultivar susceptiblility to the brown rot fungus, "Monilinia fructicola". Retrieved Sept. 19, 2014, from http://www.caf.wvu.edu/kearneysville/tables/brownrotsus.html
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20. van Brouwershaven, I. R., Bruil, M. L., van Leeuwen, G. C. M., and Kox, L. F. F. 2010. A real-time (TaqMan) PCR assay to differentiate ‘’Monilinia fructicola’’ from other brown rot fungi of fruit crops. Plant Pathology 59:548-555.
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Acknowledgements

• National Institute of Food and Agriculture, U.S. Department of Agriculture, under Agreement No. 2011-41530-30708 as part of "Diagnostic Image Series Development for Supporting IPM in the Southern Region" (USDA-NIFA-RIPM-003351)