Botrytis cinerea

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Botrytis cinerea
Aardbei Lambada vruchtrot Botrytis cinerea.jpg
Botrytis cinerea infection on strawberry
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Leotiomycetes
Order: Helotiales
Family: Sclerotiniaceae
Genus: Botrytis
Species:
B. cinerea
Binomial name
Botrytis cinerea
Pers. (1794)

Botrytis cinerea is a necrotrophic fungus that affects many plant species, although its most notable hosts may be wine grapes. In viticulture, it is commonly known as "botrytis bunch rot"; in horticulture, it is usually called "grey mould" or "gray mold".

The fungus gives rise to two different kinds of infections on grapes. The first, grey rot, is the result of consistently wet or humid conditions, and typically results in the loss of the affected bunches. The second, noble rot, occurs when drier conditions follow wetter, and can result in distinctive sweet dessert wines, such as Sauternes, the Aszú of Tokaji, or Grasă de Cotnari. [1] The species name Botrytis cinerea is derived from the Latin for "grapes like ashes"; although poetic, the "grapes" refers to the bunching of the fungal spores on their conidiophores, and "ashes" just refers to the greyish colour of the spores en masse.[ citation needed ] The fungus is usually referred to by its anamorph (asexual form) name, because the sexual phase is rarely observed. The teleomorph (sexual form) is an ascomycete, Botryotinia fuckeliana, also known as Botryotinia cinerea (see taxonomy box).

Etymology

"Botrytis" is derived from the Ancient Greek botrys (βότρυς) meaning "grapes", [2] combined with the Neo-Latin suffix -itis for disease. Botryotinia fuckeliana was named by mycologist Heinrich Anton de Bary in honor of another mycologist, Karl Wilhelm Gottlieb Leopold Fuckel. Synonyms for the sexual stage are:

Hosts and symptoms

Hosts

The disease, gray mold, affects more than 200 dicotyledonous plant species and a few monocotyledonous plants found in temperate and subtropical regions, and potentially over a thousand species. [3] [4] Serious economic losses can be a result of this disease to both field and greenhouse grown crops. The causal agent, Botrytis cinerea can infect mature or senescent tissues, plants prior to harvest, or seedlings. There is a wide variety of hosts infected by this pathogen including protein crops, fiber crops, oil crops, and horticultural crops. Horticultural crops include vegetables (examples are chickpeas, lettuce, broccoli, and beans) and small fruit crops (examples are grape, strawberry, raspberry, and blackberry [5] ), these are most severely affected and devastated by gray mold. [3] Plant organs affected include fruits, flowers, leaves, storage organs, and shoots.

Symptoms and signs

Symptoms vary across plant organs and tissues. B. cinerea is a soft rot that will have a collapsed and water soaked appearance on soft fruit and leaves. Brown lesions may develop slowly on undeveloped fruit. [6] Twigs infected with gray mold will die back. Blossoms will cause fruit drop and injury, such as ridging on developing and mature fruit. [7] Symptoms are visible at wound sites where the fungus begins to rot the plant. Gray masses with a velvety appearance are conidia on the plant tissues are a sign of plant pathogen. [7] These conidia are asexual spores that will continue to infect the plant and surrounding hosts throughout the growing season making this a polycyclic disease.

Plants can produce localized lesions when a pathogen attacks. An oxidative burst causes hypersensitive cell death called a hypersensitive response (HR). [8] This soft rot can trigger HR to assist in colonization. Botrytis cinerea, as a necrotrophic pathogen, exploits the dead tissue for its pathogenicity or its ability to cause disease. Susceptible plants cannot use the HR to protect against B. cinerea.

Biology

Conidiophore Botrytis conidiophore 40X.png
Conidiophore
Petri dish with a ring of visible sclerotia (dark brown balls) Botrytis plate.png
Petri dish with a ring of visible sclerotia (dark brown balls)

Botrytis cinerea is characterized by abundant hyaline conidia (asexual spores) borne on grey, branching tree-like conidiophores. The fungus also produces highly resistant sclerotia as survival structures in older cultures. It overwinters as sclerotia or intact mycelia, both of which germinate in spring to produce conidiophores. The conidia, dispersed by wind and by rain-water, cause new infections. B. cinerea performs an asexual cycle over the summer season.[ citation needed ]

Different strains show considerable genetic variability.[ citation needed ]

Gliocladium roseum is a fungal parasite of B. cinerea. [9]

The hypothetical protein BcKMO was shown to positively regulate growth and development. It showed a great similarity to the kynurenine 3-monooxygenase encoding gene in eukaryotes.[ citation needed ]

Overexpression of the gene atrB produces altered versions of the transcription factor mrr1 , which in turn confer a multiple fungicide resistance phenotype known as MDR1. [5] An even higher overexpression yields mrr1 composed partly of Δ497V/L, yielding MDR1h phenotypes with even more anilinopyrimidine- and phenylpyrrole- resistance. [5]

Environment

Gray mold favors moist, humid, and warm environmental conditions between 65–75 °F (18–24 °C). [10] Temperature, relative humidity, and wetness duration produce a conducive environment that is favorable for inoculation of mycelium or conidia. [11] Controlled environments, such as crop production greenhouses, provide the moisture and high temperatures that favor the spreading and development of the pathogen B. cinerea.

Standing water on plant leaf surfaces provides a place for spores to germinate. [12] Humid conditions can result from improper irrigation practice, plants placed too close together, or the structure of the greenhouse not allowing for efficient ventilation and air flow. Ventilation at night significantly reduces the incidence of gray mold. [13]

Melanized sclerotium allows B. cinerea to survive for years in the soil. Sclerotia and the asexual conidia spores contribute to the widespread infection of the pathogen. [14]

A low pH is preferred by the gray mold to perform well. B. cinerea can acidify its environment by secreting organic acids, like oxalic acid. [14] By acidifying its surroundings, cell wall degrading enzymes (CWDEs) are enhanced, plant-protection enzymes are inhibited, stomatal closure is deregulated, and pH signaling is mediated to facilitate its pathogenesis. [14]

Viticulture

Manifesting as noble rot on Riesling Botrytis riesling.jpg
Manifesting as noble rot on Riesling

In the Botrytis infection known as "noble rot" ( pourriture noble in French, or Edelfäule in German), the fungus removes water from the grapes, leaving behind a higher percent of solids, such as sugars, fruit acids and minerals. This results in a more intense, concentrated final product. The wine is often said to have an aroma of honeysuckle and a bitter finish on the palate.

A distinct fermentation process initially caused by nature, the combination of geology, climate and specific weather led to the particular balance of beneficial fungus while leaving enough of the grape intact for harvesting. The Chateau d'Yquem is the only Premier Cru Supérieur Sauternes, largely due to the vineyard's susceptibility to noble rot.

Botrytis complicates winemaking by making fermentation more complex. Botrytis produces an anti-fungal compound that kills yeast and often results in the fermentation stopping before the wine has accumulated sufficient levels of alcohol. [15]

Botrytis bunch rot is another condition of grapes caused by B. cinerea that causes great losses for the wine industry. It is always present on the fruitset, however, it requires a wound to start a bunch rot infection. Wounds can come from insects, wind, accidental damage, etc. To control botrytis bunch rot there are a number of fungicides available on the market. Generally, these should be applied at bloom, bunch closure and veraison (the most important being the bloom application). Some winemakers are known to use the German method of fermentation and prefer having a 5% bunch rot rate in their grapes and will usually hold the grapes on the vine a week longer than normal.

Horticulture

Botrytis cinerea affects many other plants.

Strawberries

It is economically important on soft fruits such as strawberries and bulb crops. [16] Unlike wine grapes, the affected strawberries are not edible and are discarded. To minimize infection in strawberry fields, good ventilation around the berries is important to prevent moisture being trapped among leaves and berries. A number of bacteria have been proven to act as natural antagonists to B. cinerea in controlled studies. [16]

Other plants

Botryotinia fuckeliana on a Goudreinet apple Botrytis-rot op appel Goudreinet (Botryotinia fuckeliana).jpg
Botryotinia fuckeliana on a Goudreinet apple

In greenhouse horticulture, Botrytis cinerea is well known as a cause of considerable damage in tomatoes.

The infection also affects rhubarb, snowdrops, white meadowfoam, western hemlock, [17] Douglas-fir, [18] cannabis, [19] [20] and Lactuca sativa . [21] UV-C treatment against B. cinerea was investigated by Vàsquez et al., 2017. They find it increases phenylalanine ammonia-lyase activity and production of phenolics. This in turn decreases L. sativa's susceptibility. [21] Potassium bicarbonate-based fungicide may be used.[ citation needed ]

Human disease

Botrytis cinerea mold on grapes may cause "winegrower's lung", a rare form of hypersensitivity pneumonitis (a respiratory allergic reaction in predisposed individuals).

Mycoviruses of Botrytis cinerea

Mycoviruses Mycoviruses of Botrytis cinerea.png
Mycoviruses

Botrytis cinerea not only infects plants, it also hosts several mycoviruses itself (see the table/image).

A range of phenotypic alterations due to the mycoviral infection have been observed from symptomless to mild impact, or more severe phenotypic changes including reduction in pathogenicity, growth/suppression of mycelia, sporulation and sclerotia production, formation of abnormal colony sectors (Wu et al., 2010 [22] ) and virulence.

Management

Botrytis cinerea can be managed through cultural, chemical, and biological practices. [23]

There are no resistant species to the gray mold rot. Gray mold can be culturally controlled by monitoring the amount and timing of fertilizer applications to reduce the amount of fruit rot. Excessive application of nitrogen will increase the incidence of disease while not improving yields. [6]

Not planting cultivars that have an upright or dense growth habit can reduce disease as these limit airflow and are favorable for the pathogen. Spacing of plants so they are not touching will increase airflow allowing the area to dry out and reduce the spread of disease. Pruning or purposeful removal of diseased, dead, or overgrown limbs on a regular schedule can also help to improve air movement. [7]

Sanitation by removing dead or dying plant tissue in the fall will decrease inoculum levels as there is no debris for the sclerotium or mycelia to overwinter. Removing debris in the spring will remove inoculum from the site. Disposal of berries during harvest that have signs and symptoms of gray mold will reduce inoculum for the following year.

Biochar, a form of charcoal, can be applied as a soil amendment to strawberry plants to reduce the severity of the fungal disease by stimulating defense pathways within the plant. [24]

Gray mold can be chemically controlled with well-timed fungicide applications starting during the first bloom. Timing can reduce the chance of resistance and will save on costs. [6]

Biological controls or microbial antagonists [ citation needed ] used for disease suppression, have been successfully used in Europe and Brazil in the form of fungi-like Trichoderma harzianum Rifai and Clonostachys rosea f. rosea Bainier (syn. Gliocladium roseum). [24] Trichoderma species especially, have been shown to control gray mold.

Multiple fungicide resistance is a problem in many production areas. [5]

See also

Related Research Articles

<i>Uncinula necator</i> Species of fungus

Uncinula necator is a fungus that causes powdery mildew of grape. It is a common pathogen of Vitis species, including the wine grape, Vitis vinifera. The fungus is believed to have originated in North America. European varieties of Vitis vinifera are more or less susceptible to this fungus. Uncinula necator infects all green tissue on the grapevine, including leaves and young berries. It can cause crop loss and poor wine quality if untreated. The sexual stage of this pathogen requires free moisture to release ascospores from its cleistothecia in the spring. However, free moisture is not needed for secondary spread via conidia; high atmospheric humidity is sufficient. Its anamorph is called Oidium tuckeri.

<span class="mw-page-title-main">Black rot (grape disease)</span> Species of fungus

Grape black rot is a fungal disease caused by an ascomycetous fungus, Guignardia bidwellii, that attacks grape vines during hot and humid weather. “Grape black rot originated in eastern North America, but now occurs in portions of Europe, South America, and Asia. It can cause complete crop loss in warm, humid climates, but is virtually unknown in regions with arid summers.” The name comes from the black fringe that borders growing brown patches on the leaves. The disease also attacks other parts of the plant, “all green parts of the vine: the shoots, leaf and fruit stems, tendrils, and fruit. The most damaging effect is to the fruit”.

<span class="mw-page-title-main">Sclerotium</span> Mycelial mass

A sclerotium, is a compact mass of hardened fungal mycelium containing food reserves. One role of sclerotia is to survive environmental extremes. In some higher fungi such as ergot, sclerotia become detached and remain dormant until favorable growth conditions return. Sclerotia initially were mistaken for individual organisms and described as separate species until Louis René Tulasne proved in 1853 that sclerotia are only a stage in the life cycle of some fungi. Further investigation showed that this stage appears in many fungi belonging to many diverse groups. Sclerotia are important in the understanding of the life cycle and reproduction of fungi, as a food source, as medicine, and in agricultural blight management.

<i>Botryotinia</i> Genus of fungi

Botryotinia is a genus of ascomycete fungi causing several plant diseases. The anamorphs of Botryotinia are mostly included in the "imperfect fungi" genus Botrytis. The genus contains 22 species and one hybrid.

Microfungi or micromycetes are fungi—eukaryotic organisms such as molds, mildews and rusts—which have microscopic spore-producing structures. They exhibit tube tip-growth and have cell walls composed of chitin, a polymer of N-acetylglucosamine. Microfungi are a paraphyletic group, distinguished from macrofungi only by the absence of a large, multicellular fruiting body. They are ubiquitous in all terrestrial and freshwater and marine environments, and grow in plants, soil, water, insects, cattle rumens, hair, and skin. Most of the fungal body consists of microscopic threads, called hyphae, extending through the substrate in which it grows. The mycelia of microfungi produce spores that are carried by the air, spreading the fungus.

<i>Monilinia laxa</i> Species of fungus

Monilinia laxa is a plant pathogen that is the causal agent of brown rot of stone fruits.

<i>Sclerotinia sclerotiorum</i> Species of fungus

Sclerotinia sclerotiorum is a plant pathogenic fungus and can cause a disease called white mold if conditions are conducive. S. sclerotiorum can also be known as cottony rot, watery soft rot, stem rot, drop, crown rot and blossom blight. A key characteristic of this pathogen is its ability to produce black resting structures known as sclerotia and white fuzzy growths of mycelium on the plant it infects. These sclerotia give rise to a fruiting body in the spring that produces spores in a sac which is why fungi in this class are called sac fungi (Ascomycota). This pathogen can occur on many continents and has a wide host range of plants. When S. sclerotiorum is onset in the field by favorable environmental conditions, losses can be great and control measures should be considered.

<i>Alternaria solani</i> Species of fungus

Alternaria solani is a fungal pathogen that produces a disease in tomato and potato plants called early blight. The pathogen produces distinctive "bullseye" patterned leaf spots and can also cause stem lesions and fruit rot on tomato and tuber blight on potato. Despite the name "early," foliar symptoms usually occur on older leaves. If uncontrolled, early blight can cause significant yield reductions. Primary methods of controlling this disease include preventing long periods of wetness on leaf surfaces and applying fungicides. Early blight can also be caused by Alternaria tomatophila, which is more virulent on stems and leaves of tomato plants than Alternaria solani.

<i>Colletotrichum coccodes</i> Pathogenic fungus

Colletotrichum coccodes is a plant pathogen, which causes anthracnose on tomato and black dot disease of potato. Fungi survive on crop debris and disease emergence is favored by warm temperatures and wet weather.

Monilinia fructigena is a plant pathogen in the fungus kingdom causing a fruit rot of apples, pears, plums, peaches and cherries.

<i>Botrytis fabae</i> Species of fungus

Botrytis fabae is a plant pathogen, a fungus that causes chocolate spot disease of broad or fava bean plants, Vicia faba. It was described scientifically by Mexican-born Galician microbiologist Juan Rodríguez Sardiña in 1929.

<i>Ulocladium</i> Genus of fungi

Ulocladium is a genus of fungi. Species of this genus contain both plant pathogens and food spoilage agents. Other species contain enzymes that are biological control agents. Some members of the genus can invade homes and are a sign of moisture because the mold requires water to thrive. They can cause plant diseases or hay fever and more serious infections in immuno-suppressed individuals.

This article summarizes different crops, what common fungal problems they have, and how fungicide should be used in order to mitigate damage and crop loss. This page also covers how specific fungal infections affect crops present in the United States.

<i>Monilinia oxycocci</i> Species of fungus

Monilinia oxycocci (Woronin) Honey,, common names cranberry cottonball, cranberry hard rot, tip blight, is a fungal infection of large cranberry and small cranberry. The tips of young flowering shoots wilt before they flower. Fruit that forms on the plant can then be infected by the asexual spores traveling through the plant, causing the berries to harden, turn cottony on the inside, and dry out instead of maturing. The berries are filled with a cotton-like fungus and are generally yellowish with tan stripes or blotches at maturity, making them unmarketable. It results in important economic impacts on many cranberry marshes, particularly in Wisconsin.

<i>Botrytis allii</i> Species of fungus

Botrytis allii is a plant pathogen, a fungus that causes neck rot in stored onions and related crops. Its teleomorph is unknown, but other species of Botrytis are anamorphs of Botryotinia species. The species was first described scientifically by Mancel Thornton Munn in 1917.

<span class="mw-page-title-main">Common spot of strawberry</span> Plant fungal disease

Common spot of strawberry is one of the most common and widespread diseases afflicting the strawberry. Common spot of strawberry is caused by the fungus Mycosphaerella fragariae. Symptoms of this disease first appear as circular, dark purple spots on the leaf surface. Mycosphaerella fragariae is very host-specific and only infects strawberry.

Cladosporium fulvum is an Ascomycete called Passalora fulva, a non-obligate pathogen that causes the disease on tomatoes known as the tomato leaf mold. P. fulva only attacks tomato plants, especially the foliage, and it is a common disease in greenhouses, but can also occur in the field. The pathogen is likely to grow in humid and cool conditions. In greenhouses, this disease causes big problems during the fall, in the early winter and spring, due to the high relative humidity of air and the temperature, that are propitious for the leaf mold development. This disease was first described in the North Carolina, by Mordecai Cubitt Cooke (1883), on cultivated tomato, although it is originally from South and Central America. The causal fungus of tomato leaf mold may also be referred to as Cladosporium fulvum, a former name.

<span class="mw-page-title-main">Thiophanate-methyl</span> Chemical compound

Thiophanate-methyl is an organic compound with the formula C6H4(NHC(S)NH(CO)OCH3)2. The compound is a colorless or white solid, although commercial samples are generally tan-colored. It is prepared from o-phenylenediamine. It is a widely used fungicide used on tree, vine, and root crops. In Europe it is applied to tomato, wine grapes, beans, wheat, and aubergine.

<i>Botrytis elliptica</i> Species of fungus

Botrytis elliptica is a necrotrophic fungal pathogen which infects species of plants in the Lilium genus, causing the disease commonly known as Lily Gray Mold. The symptoms of Lily Gray Mold include the appearance of water-soaked spots on leaves which appear white and increase in darkness with age, ranging from gray to brown. These spots may cover the entire leaf, complemented with a gray webbing, containing the fungal spores. The leaves will appear wilted and branches may die back. In addition to leaves, petals, stems, and buds may be infected, and this gray webbing will eventually cover the plant, feigning the appearance of gray flowers. Infected buds often rot. Lily Gray Mold disease, if not properly treated, will appear each year with increasing vigor.

cv. 'Camino Real' is a cultivar of strawberry produced by the Shaw & Larson era of the UC Davis breeding program.

References

  1. ↑ Richards, Helen (22 December 2014). "What is... Botrytis". JFT Wines. Retrieved 24 September 2020.
  2. ↑ βότρυς . Liddell, Henry George ; Scott, Robert ; A Greek–English Lexicon at the Perseus Project
  3. 1 2 Williamson, Brian; Tudzynski, Bettina; Tudzynski, Paul; Van Kan, Jan a. L. (2007-09-01). "Botrytis cinerea: the cause of grey mould disease". Molecular Plant Pathology. 8 (5): 561–580. doi:10.1111/j.1364-3703.2007.00417.x. ISSN   1364-3703. PMID   20507522.
  4. ↑ Fillinger, Sabine; Elad, Yigal, eds. (2016). Botrytis – the Fungus, the Pathogen and its Management in Agricultural Systems. Springer International Publishing. ISBN   978-3-319-23370-3.
  5. 1 2 3 4
  6. 1 2 3 "Botrytis Fruit Rot / Gray Mold on Strawberry | NC State Extension Publications". content.ces.ncsu.edu. Retrieved 2017-12-11.
  7. 1 2 3 "UC IPM: UC Management Guidelines for Botrytis Diseases And Disorders on Citrus". ipm.ucanr.edu. Retrieved 2017-12-11.
  8. ↑ Govrin, Eri M.; Levine, Alex (2000-06-01). "The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea". Current Biology. 10 (13): 751–757. doi: 10.1016/S0960-9822(00)00560-1 . ISSN   0960-9822. PMID   10898976. S2CID   17294773.
  9. ↑ Yu H, Sutton JC (1997). "Morphological development and interactions of Gliocladium roseum and Botrytis cinerea in raspberry" (PDF). Canadian Journal of Plant Pathology. 19 (3): 237–246. doi:10.1080/07060669709500518.[ permanent dead link ]
  10. ↑ Roberts, Pamela. "Disease Management: Gray Mold on Tomato and Ghost Spot on Pepper" (PDF). IPM Floridia. Retrieved 11 December 2017.
  11. ↑ Ciliberti, Nicola; Fermaud, Marc; Roudet, Jean; Rossi, Vittorio (August 2015). "Environmental Conditions Affect Botrytis cinerea Infection of Mature Grape Berries More Than the Strain or Transposon Genotype". Phytopathology. 105 (8): 1090–1096. doi: 10.1094/PHYTO-10-14-0264-R . hdl: 10807/69950 . ISSN   0031-949X. PMID   26218433.
  12. ↑ Physiological Aspects of Resistance to Botrytis cinerea. Elad, Y. and Evensen, K.. Publication 3 April 1995
  13. ↑ Morgan, Walter M. (1984-06-01). "The effect of night temperature and glasshouse ventilation on the incidence of Botrytis cinerea in a late-planted tomato crop". Crop Protection. 3 (2): 243–251. doi:10.1016/0261-2194(84)90058-9. ISSN   0261-2194.
  14. 1 2 3 Amselem, Joelle; Cuomo, Christina A.; Kan, Jan A. L. van; Viaud, Muriel; Benito, Ernesto P.; Couloux, Arnaud; Coutinho, Pedro M.; Vries, Ronald P. de; Dyer, Paul S. (2011-08-18). "Genomic Analysis of the Necrotrophic Fungal Pathogens Sclerotinia sclerotiorum and Botrytis cinerea". PLOS Genetics. 7 (8): e1002230. doi: 10.1371/journal.pgen.1002230 . hdl:10871/25762. ISSN   1553-7404. PMC   3158057 . PMID   21876677.
  15. ↑ van Kan, Jan A. L. (May 2006). "Licensed to kill: the lifestyle of a necrotrophic plant pathogen". Trends in Plant Science. 11 (5): 247–253. doi:10.1016/j.tplants.2006.03.005. ISSN   1360-1385. PMID   16616579.
  16. 1 2 Donmez, M. F.; Esitken, A.; Yildiz, H.; Ercisli, S. Biocontrol of Botrytis Cinerea on Strawberry Fruit by Plant Growth Promoting Bacteria, The Journal of Animal & Plant Sciences, 21(4), 2011: pp. 758-763, ISSN 1018-7081.
  17. ↑ Van Eerden, E. (1974, August). Growing season production of western conifers. In Proc. North American Containerized Forest Tree Seedling Symp., Denver, Colorado (pp. 93-103)
  18. ↑ Brix, Holger, and H. Barker. "Rooting studies of western hemlock cuttings." (1975).
  19. ↑ Lata, Hemant; ElSohly, Mahmoud A.; Chandra, Suman, eds. (2017-05-23). Cannabis Sativa L. - Botany and Biotechnology. Cham, Switzerland: Springer International. p. 275. ISBN   978-3-319-54563-9. Cannabis is highly susceptible to diseases caused by fungal growth. Densely packed buds and flowering tops hold high content of moisture that allows for infestation by molds such as Botrytis cinerea, Sclerotinia sclerotiorum, Fusarium species etc.
  20. ↑ McPartland, JM; Clarke, RC; Watson, DP (2000). Hemp Diseases and Pests: Management and Biological Control: An Advanced Treatise. Wallingford, United Kingdom: CABI. p. 95. B. cinera often colonizes senescent leaves and flowers, and from these footholds it invades the rest of the plant.
  21. 1 2 Urban, L.; Chabane Sari, D.; Orsal, B.; Lopes, M.; Miranda, R.; Aarrouf, J. (2018). "UV-C light and pulsed light as alternatives to chemical and biological elicitors for stimulating plant natural defenses against fungal diseases". Scientia Horticulturae . 235. Elsevier: 452–459. doi:10.1016/j.scienta.2018.02.057. ISSN   0304-4238. S2CID   90436989.
  22. ↑ Wu M. D.; Zhang L.; Li G.; Jiang D.; Ghabrial S. A. (2010). "Genome characterization of a debilitation-associated mitovirus infecting the phytopathogenic fungus Botrytis cinerea". Virology. 406 (1): 117–126. doi: 10.1016/j.virol.2010.07.010 . PMID   20674953.
  23. ↑ McLoughlin, Austein G.; Wytinck, Nick; Walker, Philip L.; Girard, Ian J.; Rashid, Khalid Y.; Kievit, Teresa de; Fernando, W. G. Dilantha; Whyard, Steve; Belmonte, Mark F. (9 May 2018). "Identification and application of exogenous dsRNA confers plant protection against Sclerotinia sclerotiorum and Botrytis cinerea". Sci Rep. 8 (1): 7320. Bibcode:2018NatSR...8.7320M. doi:10.1038/s41598-018-25434-4. PMC   5943259 . PMID   29743510.
  24. 1 2 Harel, Yael Meller; Elad, Yigal; Rav-David, Dalia; Borenstein, Menachem; Shulchani, Ran; Lew, Beni; Graber, Ellen R. (2012). "Biochar mediates systemic response of strawberry to foliar fungal pathogens". Plant and Soil. 357 (1–2): 245–257. doi:10.1007/s11104-012-1129-3. JSTOR   24370313. S2CID   16186999.
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